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20 pages, 3280 KiB

Open AccessArticle

Zeta-Carotene Isomerase (Z-ISO) Is Required for Light-Independent Carotenoid Biosynthesis in the Cyanobacterium Synechocystis sp. PCC 6803

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Matthew S. Proctor

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Felix S. Morey-Burrows

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Daniel P. Canniffe

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Elizabeth C. Martin

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David J. K. Swainsbury

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Microorganisms 2022, 10(9), 1730; https://doi.org/10.3390/microorganisms10091730 - 27 Aug 2022

Cited by 2 | Viewed by 1602

Abstract

Carotenoids are crucial photosynthetic pigments utilized for light harvesting, energy transfer, and photoprotection. Although most of the enzymes involved in carotenoid biosynthesis in chlorophototrophs are known, some are yet to be identified or fully characterized in certain organisms. A recently characterized enzyme in [...] Read more.

Carotenoids are crucial photosynthetic pigments utilized for light harvesting, energy transfer, and photoprotection. Although most of the enzymes involved in carotenoid biosynthesis in chlorophototrophs are known, some are yet to be identified or fully characterized in certain organisms. A recently characterized enzyme in oxygenic phototrophs is 15-cis-zeta(ζ)-carotene isomerase (Z-ISO), which catalyzes the cis-to-trans isomerization of the central 15–15′ cis double bond in 9,15,9′-tri-cis-ζ-carotene to produce 9,9′-di-cis-ζ-carotene during the four-step conversion of phytoene to lycopene. Z-ISO is a heme B-containing enzyme best studied in angiosperms. Homologs of Z-ISO are present in organisms that use the multi-enzyme poly-cis phytoene desaturation pathway, including algae and cyanobacteria, but appear to be absent in green bacteria. Here we confirm the identity of Z-ISO in the model unicellular cyanobacterium Synechocystis sp. PCC 6803 by showing that the protein encoded by the slr1599 open reading frame has ζ-carotene isomerase activity when produced in Escherichia coli. A Synechocystis Δslr1599 mutant synthesizes a normal quota of carotenoids when grown under illumination, where the photolabile 15–15′ cis double bond of 9,15,9′-tri-cis-ζ-carotene is isomerized by light, but accumulates this intermediate and fails to produce ‘mature’ carotenoid species during light-activated heterotrophic growth, demonstrating the requirement of Z-ISO for carotenoid biosynthesis during periods of darkness. In the absence of a structure of Z-ISO, we analyze AlphaFold models of the Synechocystis, Zea mays (maize), and Arabidopsis thaliana enzymes, identifying putative protein ligands for the heme B cofactor and the substrate-binding site. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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20 pages, 2926 KiB

Open AccessArticle

Seasonal Dynamics of Lake Winnipeg’s Microbial Communities Reveal Aerobic Anoxygenic Phototrophic Populations Coincide with Sunlight Availability

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Steven B. Kuzyk

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Xiao Ma

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Vladimir Yurkov

Microorganisms 2022, 10(9), 1690; https://doi.org/10.3390/microorganisms10091690 - 23 Aug 2022

Cited by 1 | Viewed by 1392

Abstract

In this first comprehensive study of Lake Winnipeg’s microbial communities, limnetic and littoral euphotic zones were examined during each season from 2016 through 2020. Classical cultivation and modern high-throughput sequencing techniques provided quantification and identification of key phototrophic populations, including aerobic anoxygenic phototrophs [...] Read more.

In this first comprehensive study of Lake Winnipeg’s microbial communities, limnetic and littoral euphotic zones were examined during each season from 2016 through 2020. Classical cultivation and modern high-throughput sequencing techniques provided quantification and identification of key phototrophic populations, including aerobic anoxygenic phototrophs (AAP). Annual dynamics found total heterotrophs reached 4.23 × 10⁶ CFU/g in littoral sands, and 7.69 × 10⁴ CFU/mL in summer littoral waters on oligotrophic media, higher counts than for copiotrophic compositions. Limnetic numbers inversely dipped to 4.34 × 10³ CFU/mL midsummer. Cultured AAP did not follow heterotrophic trends, instead peaking during the spring in both littoral and limnetic waters as 19.1 and 4.7% of total copiotrophs, or 3.9 and 4.9% of oligotrophs, decreasing till autumn each year. Complementary observations came from environmental 16S V4 rRNA gene analysis, as AAP made up 1.49 and 1.02% of the littoral and limnetic sequenced communities in the spring, declining with seasonal progression. Spatial and temporal fluctuations of microbes compared to environmental factors exposed photosynthetic populations to independently and regularly fluctuate in the ecosystem. Oxygenic phototrophic numbers expectantly matched the midsummer peak of Chl a and b, oxygenic photosynthesis related carbon fixation, and water temperature. Independently, AAP particularly colonized spring littoral areas more than limnetic, and directly corresponded to habitat conditions that specifically promoted growth: the requirement of light and organic material. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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21 pages, 3590 KiB

Open AccessArticle

Evidence for Electron Transfer from the Bidirectional Hydrogenase to the Photosynthetic Complex I (NDH-1) in the Cyanobacterium Synechocystis sp. PCC 6803

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Microorganisms 2022, 10(8), 1617; https://doi.org/10.3390/microorganisms10081617 - 10 Aug 2022

Cited by 1 | Viewed by 1944

Abstract

The cyanobacterial bidirectional [NiFe]-hydrogenase is a pentameric enzyme. Apart from the small and large hydrogenase subunits (HoxYH) it contains a diaphorase module (HoxEFU) that interacts with NAD(P)⁺ and ferredoxin. HoxEFU shows strong similarity to the outermost subunits (NuoEFG) of canonical respiratory complexes [...] Read more.

The cyanobacterial bidirectional [NiFe]-hydrogenase is a pentameric enzyme. Apart from the small and large hydrogenase subunits (HoxYH) it contains a diaphorase module (HoxEFU) that interacts with NAD(P)⁺ and ferredoxin. HoxEFU shows strong similarity to the outermost subunits (NuoEFG) of canonical respiratory complexes I. Photosynthetic complex I (NDH-1) lacks these three subunits. This led to the idea that HoxEFU might interact with NDH-1 instead. HoxEFUYH utilizes excited electrons from PSI for photohydrogen production and it catalyzes the reverse reaction and feeds electrons into the photosynthetic electron transport. We analyzed hydrogenase activity, photohydrogen evolution and hydrogen uptake, the respiration and photosynthetic electron transport of ΔhoxEFUYH, and a knock-out strain with dysfunctional NDH-1 (ΔndhD1/ΔndhD2) of the cyanobacterium Synechocystis sp. PCC 6803. Photohydrogen production was prolonged in ΔndhD1/ΔndhD2 due to diminished hydrogen uptake. Electrons from hydrogen oxidation must follow a different route into the photosynthetic electron transport in this mutant compared to wild type cells. Furthermore, respiration was reduced in ΔhoxEFUYH and the ΔndhD1/ΔndhD2 localization of the hydrogenase to the membrane was impaired. These data indicate that electron transfer from the hydrogenase to the NDH-1 complex is either direct, by the binding of the hydrogenase to the complex, or indirect, via an additional mediator. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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12 pages, 8103 KiB

Open AccessArticle

Nitrogen Fixation Activity and Genome Analysis of a Moderately Haloalkaliphilic Anoxygenic Phototrophic Bacterium Rhodovulum tesquicola

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Anastasia V. Komova

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Elizaveta D. Bakhmutova

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Aleksei A. Korzhenkov

Microorganisms 2022, 10(8), 1615; https://doi.org/10.3390/microorganisms10081615 - 09 Aug 2022

Viewed by 1408

Abstract

The genome of the moderately haloalkaliphilic diazotrophic anoxygenic phototrophic bacterium Rhodovulum tesquicola A-36s^T isolated from an alkaline lake was analyzed and compared to the genomes of the closest species Rhodovulum steppense A-20s^T and Rhodovulum strictum DSM 11289^T. The genomic [...] Read more.

The genome of the moderately haloalkaliphilic diazotrophic anoxygenic phototrophic bacterium Rhodovulum tesquicola A-36s^T isolated from an alkaline lake was analyzed and compared to the genomes of the closest species Rhodovulum steppense A-20s^T and Rhodovulum strictum DSM 11289^T. The genomic features of three organisms are quite similar, reflecting their ecological and physiological role of facultative photoheterotrophs. Nevertheless, the nitrogenase activity of the pure cultures of the studied bacteria differed significantly: the highest rate (4066 nmoles C₂H₂/mg of dry weight per hour) was demonstrated by Rhodovulum strictum while the rates in Rhodovulum tesquicola and Rhodovulum steppense were an order of magnitude lower (278 and 523 nmoles C₂H₂/mg of dry weight per hour, respectively). This difference can be attributed to the presence of an additional nitrogenase operon found exclusively in R. strictum and to the structural variation in nitrogenase operon in R. tesquicola. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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15 pages, 3531 KiB

Open AccessArticle

Chromatic Acclimation Processes and Their Relationships with Phycobiliprotein Complexes

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Fanyue Wang

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Min Chen

Microorganisms 2022, 10(8), 1562; https://doi.org/10.3390/microorganisms10081562 - 03 Aug 2022

Cited by 4 | Viewed by 1321

Abstract

Chromatic acclimation (CA) is a widespread mechanism for optimizing the composition of phycobiliprotein complexes to maximize the cyanobacterial light capture efficiency. There are seven CA types, CA1-CA7, classified according to various photoregulatory pathways. Here, we use sequence analyses and bioinformatics to predict the [...] Read more.

Chromatic acclimation (CA) is a widespread mechanism for optimizing the composition of phycobiliprotein complexes to maximize the cyanobacterial light capture efficiency. There are seven CA types, CA1-CA7, classified according to various photoregulatory pathways. Here, we use sequence analyses and bioinformatics to predict the presence of CA types according to three GAF (cGMP phosphodiesterase/adenylyl cyclase/FhlA)-containing photoreceptors, CcaS (cyanobacterial chromatic acclimation sensor), RcaE (regulator of chromatic adaptation), and RfpA (regulator for far-red photoacclimation). These photoreceptors were classified into three different phylogenetic groups leading different CA types in a diverse range of cyanobacteria. Combining with genomic information of phycobilisome compositions, the CA capabilities of various cyanobacteria were conjectured. Screening 65 accessible cyanobacterial genomes, we defined 19 cyanobacteria that have the capability to perform far-red light photoacclimation (FaRLiP) under the control of RfpA. Forty out of sixty-five cyanobacteria have the capability to perform green/red light photoacclimation, although they use different photoreceptors (RcaE and/or CcaS) and photoregulatory pathways. The reversible response of photoreceptors in CA regulation pathways trigged by changed light conditions reflects the flexibility of photoregulatory mechanisms in cyanobacteria and the putative independent evolutionary origin of photoacclimation types. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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16 pages, 1779 KiB

Open AccessArticle

Comparative Genomic Analysis of the Marine Cyanobacterium Acaryochloris marina MBIC10699 Reveals the Impact of Phycobiliprotein Reacquisition and the Diversity of Acaryochloris Plasmids

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Microorganisms 2022, 10(7), 1374; https://doi.org/10.3390/microorganisms10071374 - 07 Jul 2022

Cited by 2 | Viewed by 1424

Abstract

Acaryochloris is a marine cyanobacterium that synthesizes chlorophyll d, a unique chlorophyll that absorbs far-red lights. Acaryochloris is also characterized by the loss of phycobiliprotein (PBP), a photosynthetic antenna specific to cyanobacteria; however, only the type-strain A. marina MBIC11017 retains PBP, suggesting [...] Read more.

Acaryochloris is a marine cyanobacterium that synthesizes chlorophyll d, a unique chlorophyll that absorbs far-red lights. Acaryochloris is also characterized by the loss of phycobiliprotein (PBP), a photosynthetic antenna specific to cyanobacteria; however, only the type-strain A. marina MBIC11017 retains PBP, suggesting that PBP-related genes were reacquired through horizontal gene transfer (HGT). Acaryochloris is thought to have adapted to various environments through its huge genome size and the genes acquired through HGT; however, genomic information on Acaryochloris is limited. In this study, we report the complete genome sequence of A. marina MBIC10699, which was isolated from the same area of ocean as A. marina MBIC11017 as a PBP-less strain. The genome of A.marina MBIC10699 consists of a 6.4 Mb chromosome and four large plasmids totaling about 7.6 Mb, and the phylogenic analysis shows that A.marina MBIC10699 is the most closely related to A. marina MBIC11017 among the Acaryochloris species reported so far. Compared with A. marina MBIC11017, the chromosomal genes are highly conserved between them, while the genes encoded in the plasmids are significantly diverse. Comparing these genomes provides clues as to how the genes for PBPs were reacquired and what changes occurred in the genes for photosystems during evolution. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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16 pages, 3354 KiB

Open AccessArticle

Attachment of Ferredoxin: NADP⁺ Oxidoreductase to Phycobilisomes Is Required for Photoheterotrophic Growth of the Cyanobacterium Synechococcus sp. PCC 7002

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Microorganisms 2022, 10(7), 1313; https://doi.org/10.3390/microorganisms10071313 - 29 Jun 2022

Cited by 3 | Viewed by 1536

Abstract

Two types of cyanobacterial phycobilisomes (PBS) are present: the hemidiscoidal PBS (CpcG-PBS) and the membrane-bound PBS (CpcL-PBS). Both types of PBS have ferredoxin:NADP⁺ oxidoreductase (FNR) attached to the termini of their rods through a CpcD domain. To date, the physiological significance of [...] Read more.

Two types of cyanobacterial phycobilisomes (PBS) are present: the hemidiscoidal PBS (CpcG-PBS) and the membrane-bound PBS (CpcL-PBS). Both types of PBS have ferredoxin:NADP⁺ oxidoreductase (FNR) attached to the termini of their rods through a CpcD domain. To date, the physiological significance of the attachment remains unknown. We constructed a mutant (dF338) which contains an FNR lacking the N-terminal CpcD domain in Synechococcus sp. PCC 7002. Isolated CpcG-PBS from dF338 did not contain FNR and the cell extracts of the mutant had a 35 kDa protein cross-reacting to anti-FNR antibodies. dF338 grows normally under photoautotrophic conditions, but little growth was observed under photoheterotrophic conditions. A cpcL (cpcG2) mutant grows extremely slowly under photoheterotrophic conditions while a cpcG (cpcG1) mutant, in which PBS rods could not attach to the cores of the CpcG-PBS, can grow photoheterotrophically, strongly suggesting that the attachment of FNR to CpcL-PBS is critical to photoheterotrophic growth. We show that electron transfer to the plastoquinone pool in dF338 and the cpcL mutant was impaired. We also provide evidence that trimeric photosystem I (PSI) and intact CpcL-PBS with a full-length FNR is critical to plastoquinone reduction. The presence of a NADPH-dehydrogenase (NDH)-CpcL-PBS-PSI trimer supercomplex and its roles are discussed. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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25 pages, 6039 KiB

Open AccessArticle

Phylogenomic Analyses and Molecular Signatures Elucidating the Evolutionary Relationships amongst the Chlorobia and Ignavibacteria Species: Robust Demarcation of Two Family-Level Clades within the Order Chlorobiales and Proposal for the Family Chloroherpetonaceae fam. nov

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Sarah Bello

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Mohammad Howard-Azzeh

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Herb E. Schellhorn

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Radhey S. Gupta

Microorganisms 2022, 10(7), 1312; https://doi.org/10.3390/microorganisms10071312 - 29 Jun 2022

Cited by 4 | Viewed by 1543

Abstract

Evolutionary relationships amongst Chlorobia and Ignavibacteria species/strains were examined using phylogenomic and comparative analyses of genome sequences. In a phylogenomic tree based on 282 conserved proteins, the named Chlorobia species formed a monophyletic clade containing two distinct subclades. One clade, encompassing the genera [...] Read more.

Evolutionary relationships amongst Chlorobia and Ignavibacteria species/strains were examined using phylogenomic and comparative analyses of genome sequences. In a phylogenomic tree based on 282 conserved proteins, the named Chlorobia species formed a monophyletic clade containing two distinct subclades. One clade, encompassing the genera Chlorobaculum, Chlorobium, Pelodictyon, and Prosthecochloris, corresponds to the family Chlorobiaceae, whereas another clade, harboring Chloroherpeton thalassium, Candidatus Thermochlorobacter aerophilum, Candidatus Thermochlorobacteriaceae bacterium GBChlB, and Chlorobium sp. 445, is now proposed as a new family (Chloroherpetonaceae fam. nov). In parallel, our comparative genomic analyses have identified 47 conserved signature indels (CSIs) in diverse proteins that are exclusively present in members of the class Chlorobia or its two families, providing reliable means for identification. Two known Ignavibacteria species in our phylogenomic tree are found to group within a larger clade containing several Candidatus species and uncultured Chlorobi strains. A CSI in the SecY protein is uniquely shared by the species/strains from this “larger Ignavibacteria clade”. Two additional CSIs, which are commonly shared by Chlorobia species and the “larger Ignavibacteria clade”, support a specific relationship between these two groups. The newly identified molecular markers provide novel tools for genetic and biochemical studies and identification of these organisms. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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15 pages, 4683 KiB

Open AccessArticle

Proteomic Time-Course Analysis of the Filamentous Anoxygenic Phototrophic Bacterium, Chloroflexus aurantiacus, during the Transition from Respiration to Phototrophy

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Microorganisms 2022, 10(7), 1288; https://doi.org/10.3390/microorganisms10071288 - 25 Jun 2022

Cited by 1 | Viewed by 1654

Abstract

Chloroflexus aurantiacus is a filamentous anoxygenic phototrophic bacterium that grows chemotrophically under oxic conditions and phototrophically under anoxic conditions. Because photosynthesis-related genes are scattered without any gene clusters in the genome, it is still unclear how this bacterium regulates protein expression in response [...] Read more.

Chloroflexus aurantiacus is a filamentous anoxygenic phototrophic bacterium that grows chemotrophically under oxic conditions and phototrophically under anoxic conditions. Because photosynthesis-related genes are scattered without any gene clusters in the genome, it is still unclear how this bacterium regulates protein expression in response to environmental changes. In this study, we performed a proteomic time-course analysis of how C. aurantiacus expresses proteins to acclimate to environmental changes, namely the transition from chemoheterotrophic respiratory to photoheterotrophic growth mode. Proteomic analysis detected a total of 2520 proteins out of 3934 coding sequences in the C. aurantiacus genome from samples collected at 13 time points. Almost all proteins for reaction centers, light-harvesting chlorosomes, and carbon fixation pathways were successfully detected during the growing phases in which optical densities and relative bacteriochlorophyll c contents increased simultaneously. Combination of proteomics and pigment analysis suggests that the self-aggregation of bacteriochlorophyllide c could precede the esterification of the hydrophobic farnesyl tail in cells. Cytoplasmic subunits of alternative complex III were interchanged between oxic and anoxic conditions, although membrane-bound subunits were used for both conditions. These data highlight the protein expression dynamics of phototrophy-related genes during the transition from respiration to phototrophy. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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18 pages, 33059 KiB

Open AccessArticle

Molecular Evolution of Far-Red Light-Acclimated Photosystem II

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Christopher J. Gisriel

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Tanai Cardona

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Donald A. Bryant

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Gary W. Brudvig

Microorganisms 2022, 10(7), 1270; https://doi.org/10.3390/microorganisms10071270 - 22 Jun 2022

Cited by 8 | Viewed by 2236

Abstract

Cyanobacteria are major contributors to global carbon fixation and primarily use visible light (400−700 nm) to drive oxygenic photosynthesis. When shifted into environments where visible light is attenuated, a small, but highly diverse and widespread number of cyanobacteria can express modified pigments and [...] Read more.

Cyanobacteria are major contributors to global carbon fixation and primarily use visible light (400−700 nm) to drive oxygenic photosynthesis. When shifted into environments where visible light is attenuated, a small, but highly diverse and widespread number of cyanobacteria can express modified pigments and paralogous versions of photosystem subunits and phycobiliproteins that confer far-red light (FRL) absorbance (700−800 nm), a process termed far-red light photoacclimation, or FaRLiP. During FaRLiP, alternate photosystem II (PSII) subunits enable the complex to bind chlorophylls d and f, which absorb at lower energy than chlorophyll a but still support water oxidation. How the FaRLiP response arose remains poorly studied. Here, we report ancestral sequence reconstruction and structure-based molecular evolutionary studies of the FRL-specific subunits of FRL-PSII. We show that the duplications leading to the origin of two PsbA (D1) paralogs required to make chlorophyll f and to bind chlorophyll d in water-splitting FRL-PSII are likely the first to have occurred prior to the diversification of extant cyanobacteria. These duplications were followed by those leading to alternative PsbC (CP43) and PsbD (D2) subunits, occurring early during the diversification of cyanobacteria, and culminating with those leading to PsbB (CP47) and PsbH paralogs coincident with the radiation of the major groups. We show that the origin of FRL-PSII required the accumulation of a relatively small number of amino acid changes and that the ancestral FRL-PSII likely contained a chlorophyll d molecule in the electron transfer chain, two chlorophyll f molecules in the antenna subunits at equivalent positions, and three chlorophyll a molecules whose site energies were altered. The results suggest a minimal model for engineering far-red light absorbance into plant PSII for biotechnological applications. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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17 pages, 3912 KiB

Open AccessArticle

Taxonomic Re-Evaluation and Genomic Comparison of Novel Extracellular Electron Uptake-Capable Rhodovulum visakhapatnamense and Rhodovulum sulfidophilum Isolates

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Emily J. Davenport

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Arpita Bose

Microorganisms 2022, 10(6), 1235; https://doi.org/10.3390/microorganisms10061235 - 16 Jun 2022

Cited by 1 | Viewed by 1664

Abstract

Rhodovulum spp. are anoxygenic phototrophic purple bacteria with versatile metabolisms, including the ability to obtain electrons from minerals in their environment to drive photosynthesis, a relatively novel process called phototrophic extracellular electron uptake (pEEU). A total of 15 strains of Rhodovulum sulfidophilum were [...] Read more.

Rhodovulum spp. are anoxygenic phototrophic purple bacteria with versatile metabolisms, including the ability to obtain electrons from minerals in their environment to drive photosynthesis, a relatively novel process called phototrophic extracellular electron uptake (pEEU). A total of 15 strains of Rhodovulum sulfidophilum were isolated from a marine estuary to observe these metabolisms in marine phototrophs. One representative strain, Rhodovulum sulfidophilum strain AB26, can perform phototrophic iron oxidation (photoferrotrophy) and couples carbon dioxide fixation to pEEU. Here, we reclassify two R. sulfidophilum isolates, strainAB26 and strain AB19, as Rhodovulum visakhapatnamense using taxonomic re-evaluation based on 16S and pufM phylogenetic analyses. The strain AB26 genome consists of 4,380,746 base-pairs, including two plasmids, and encodes 4296 predicted protein-coding genes. Strain AB26 contains 22 histidine kinases, 20 response regulators, and dedicates ~16% of its genome to transport. Transcriptomic data under aerobic, photoheterotrophy, photoautotrophy, and pEEU reveals how gene expression varies between metabolisms in a novel R. visakhapatnamense strain. Genome comparison led by transcriptomic data under pEEU reveals potential pEEU-relevant genes both unique to R. visakhapatnamense strains and shared within the R. sulfidophilum genomes. With these data we identify potential pEEU-important transcripts and how speciation may affect molecular mechanisms of pEEU in Rhodovulum species from the same environment. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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10 pages, 1855 KiB

Open AccessArticle

Translational Frameshifting in the chlD Gene Gives a Clue to the Coevolution of the Chlorophyll and Cobalamin Biosyntheses

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Stepan Kuznetsov

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Alexander Milenkin

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Ivan Antonov

Microorganisms 2022, 10(6), 1200; https://doi.org/10.3390/microorganisms10061200 - 11 Jun 2022

Viewed by 1172

Abstract

Today, hundreds of prokaryotic species are able to synthesize chlorophyll and cobalamin (vitamin B12). An important step in the biosynthesis of these coenzymes is the insertion of a metal ion into a porphyrin ring. Namely, Mg-chelatase ChlIDH and aerobic Co-chelatase CobNST are utilized [...] Read more.

Today, hundreds of prokaryotic species are able to synthesize chlorophyll and cobalamin (vitamin B12). An important step in the biosynthesis of these coenzymes is the insertion of a metal ion into a porphyrin ring. Namely, Mg-chelatase ChlIDH and aerobic Co-chelatase CobNST are utilized in the chlorophyll and vitamin B12 pathways, respectively. The corresponding subunits of these enzymes have common evolutionary origin. Recently, we have identified a highly conserved frameshifting signal in the chlD gene. This unusual regulatory mechanism allowed production of both the small and the medium chelatase subunits from the same gene. Moreover, the chlD gene appeared early in the evolution and could be at the starting point in the development of the chlorophyll and B12 pathways. Here, we studied the possible coevolution of these two pathways through the analysis of the chelatase genes. To do that, we developed a specialized Web database with comprehensive information about more than 1200 prokaryotic genomes. Further analysis allowed us to split the coevolution of the chlorophyll and B12 pathway into eight distinct stages. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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20 pages, 2622 KiB

Open AccessArticle

Genome Sequence and Characterization of a Xanthorhodopsin-Containing, Aerobic Anoxygenic Phototrophic Rhodobacter Species, Isolated from Mesophilic Conditions at Yellowstone National Park

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John A. Kyndt

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Sydney Robertson

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Isabella B. Shoffstall

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Robert F. Ramaley

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Terrance E. Meyer

Microorganisms 2022, 10(6), 1169; https://doi.org/10.3390/microorganisms10061169 - 07 Jun 2022

Cited by 3 | Viewed by 1914

Abstract

The genus Rhodobacter consists of purple nonsulfur photosynthetic alphaproteobacteria known for their diverse metabolic capabilities. Here, we report the genome sequence and initial characterization of a novel Rhodobacter species, strain M37P, isolated from Mushroom hot spring runoff in Yellowstone National Park at 37 [...] Read more.

The genus Rhodobacter consists of purple nonsulfur photosynthetic alphaproteobacteria known for their diverse metabolic capabilities. Here, we report the genome sequence and initial characterization of a novel Rhodobacter species, strain M37P, isolated from Mushroom hot spring runoff in Yellowstone National Park at 37 °C. Genome-based analyses and initial growth characteristics helped to define the differentiating characteristics of this species and identified it as an aerobic anoxygenic phototroph (AAP). This is the first AAP identified in the genus Rhodobacter. Strain M37P has a pinkish-red pigmentation that is present under aerobic dark conditions but disappears under light incubation. Whole genome-based analysis and average nucleotide identity (ANI) comparison indicate that strain M37P belongs to a specific clade of recently identified species that are genetically and physiologically unique from other representative Rhodobacter species. The genome encodes a unique xanthorhodopsin, not found in any other Rhodobacter species, which may be responsible for the pinkish-red pigmentation. These analyses indicates that strain M37P is a unique species that is well-adapted to optimized growth in the Yellowstone hot spring runoff, for which we propose the name Rhodobacter calidifons sp. nov. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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16 pages, 3623 KiB

Open AccessArticle

Zam Is a Redox-Regulated Member of the RNB-Family Required for Optimal Photosynthesis in Cyanobacteria

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Patrick E. Thomas

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Colin Gates

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William Campodonico-Burnett

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Jeffrey C. Cameron

Microorganisms 2022, 10(5), 1055; https://doi.org/10.3390/microorganisms10051055 - 20 May 2022

Viewed by 1782

Abstract

The zam gene mediating resistance to acetazolamide in cyanobacteria was discovered thirty years ago during a drug tolerance screen. We use phylogenetics to show that Zam proteins are distributed across cyanobacteria and that they form their own unique clade of the ribonuclease II/R [...] Read more.

The zam gene mediating resistance to acetazolamide in cyanobacteria was discovered thirty years ago during a drug tolerance screen. We use phylogenetics to show that Zam proteins are distributed across cyanobacteria and that they form their own unique clade of the ribonuclease II/R (RNB) family. Despite being RNB family members, multiple sequence alignments reveal that Zam proteins lack conservation and exhibit extreme degeneracy in the canonical active site—raising questions about their cellular function(s). Several known phenotypes arise from the deletion of zam, including drug resistance, slower growth, and altered pigmentation. Using room-temperature and low-temperature fluorescence and absorption spectroscopy, we show that deletion of zam results in decreased phycocyanin synthesis rates, altered PSI:PSII ratios, and an increase in coupling between the phycobilisome and PSII. Conserved cysteines within Zam are identified and assayed for function using in vitro and in vivo methods. We show that these cysteines are essential for Zam function, with mutation of either residue to serine causing phenotypes identical to the deletion of Zam. Redox regulation of Zam activity based on the reversible oxidation-reduction of a disulfide bond involving these cysteine residues could provide a mechanism to integrate the ‘central dogma’ with photosynthesis in cyanobacteria. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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16 pages, 4552 KiB

Open AccessArticle

A Cyanobacteria Enriched Layer of Shark Bay Stromatolites Reveals a New Acaryochloris Strain Living in Near Infrared Light

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Unnikrishnan Kuzhiumparambil

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Lisa M. Sedger

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Anthony W. D. Larkum

Microorganisms 2022, 10(5), 1035; https://doi.org/10.3390/microorganisms10051035 - 17 May 2022

Viewed by 2078

Abstract

The genus Acaryochloris is unique among phototrophic organisms due to the dominance of chlorophyll d in its photosynthetic reaction centres and light-harvesting proteins. This allows Acaryochloris to capture light energy for photosynthesis over an extended spectrum of up to ~760 nm in the [...] Read more.

The genus Acaryochloris is unique among phototrophic organisms due to the dominance of chlorophyll d in its photosynthetic reaction centres and light-harvesting proteins. This allows Acaryochloris to capture light energy for photosynthesis over an extended spectrum of up to ~760 nm in the near infra-red (NIR) spectrum. Acaryochloris sp. has been reported in a variety of ecological niches, ranging from polar to tropical shallow aquatic sites. Here, we report a new Acarychloris strain isolated from an NIR-enriched stratified microbial layer 4–6 mm under the surface of stromatolite mats located in the Hamelin Pool of Shark Bay, Western Australia. Pigment analysis by spectrometry/fluorometry, flow cytometry and spectral confocal microscopy identifies unique patterns in pigment content that likely reflect niche adaption. For example, unlike the original A. marina species (type strain MBIC11017), this new strain, Acarychloris LARK001, shows little change in the chlorophyll d/a ratio in response to changes in light wavelength, displays a different Fv/Fm response and lacks detectable levels of phycocyanin. Indeed, 16S rRNA analysis supports the identity of the A. marina LARK001 strain as close to but distinct from from the A. marina HICR111A strain first isolated from Heron Island and previously found on the Great Barrier Reef under coral rubble on the reef flat. Taken together, A. marina LARK001 is a new cyanobacterial strain adapted to the stromatolite mats in Shark Bay. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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12 pages, 2148 KiB

Open AccessArticle

Salt- and pH-Dependent Thermal Stability of Photocomplexes from Extremophilic Bacteriochlorophyll b-Containing Halorhodospira Species

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Microorganisms 2022, 10(5), 959; https://doi.org/10.3390/microorganisms10050959 - 02 May 2022

Cited by 1 | Viewed by 1516

Abstract

Halorhodospira (Hlr.) species are the most halophilic and alkaliphilic of all purple bacteria. Hlr. halochloris exhibits the lowest LH1 Q_y transition energy among phototrophic organisms and is the only known triply extremophilic anoxygenic phototroph, displaying a thermophilic, halophilic, and alkaliphilic [...] Read more.

Halorhodospira (Hlr.) species are the most halophilic and alkaliphilic of all purple bacteria. Hlr. halochloris exhibits the lowest LH1 Q_y transition energy among phototrophic organisms and is the only known triply extremophilic anoxygenic phototroph, displaying a thermophilic, halophilic, and alkaliphilic phenotype. Recently, we reported that electrostatic charges are responsible for the unusual spectroscopic properties of the Hlr. halochloris LH1 complex. In the present work, we examined the effects of salt and pH on the spectroscopic properties and thermal stability of LH1-RCs from Hlr. halochloris compared with its mesophilic counterpart, Hlr. abdelmalekii. Experiments in which the photocomplexes were subjected to different levels of salt or variable pH revealed that the thermal stability of LH1-RCs from both species was largely retained in the presence of high salt concentrations and/or at alkaline pH but was markedly reduced by lowering the salt concentration and/or pH. Based on the amino acid sequences of LH1 polypeptides and their composition of acidic/basic residues and the Hofmeister series for cation/anion species, we discuss the importance of electrostatic charge in stabilizing the Hlr. halochloris LH1-RC complex to allow it to perform photosynthesis in its warm, hypersaline, and alkaline habitat. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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13 pages, 3521 KiB

Open AccessArticle

The Response Regulator RegA Is a Copper Binding Protein That Covalently Dimerizes When Exposed to Oxygen

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Nijia Ke

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Carl E. Bauer

Microorganisms 2022, 10(5), 934; https://doi.org/10.3390/microorganisms10050934 - 29 Apr 2022

Viewed by 1295

Abstract

In Rhodobacter capsulatus, the histidine kinase RegB is believed to phosphorylate its cognate transcriptional factor RegA only under anaerobic conditions. However, transcriptome evidence indicates that RegA regulates 47 genes involved in energy storage, energy production, signaling and transcription, under aerobic conditions. In [...] Read more.

In Rhodobacter capsulatus, the histidine kinase RegB is believed to phosphorylate its cognate transcriptional factor RegA only under anaerobic conditions. However, transcriptome evidence indicates that RegA regulates 47 genes involved in energy storage, energy production, signaling and transcription, under aerobic conditions. In this study, we provide evidence that RegA is a copper binding protein and that copper promotes the dimerization of RegA under aerobic conditions. Inductively coupled plasma mass spectrometry (ICP-MS) analysis indicates that RegA binds Cu¹⁺ and Cu²⁺ in a 1:1 and 2:1 ratio, respectively. Through LC-MS/MS, ESI-MS and non-reducing SDS-PAGE gels, we show that Cu²⁺ stimulates disulfide bond formation in RegA at Cys156 in the presence of oxygen. Finally, we used DNase I footprint analysis to demonstrate that Cu²⁺-mediated covalent dimerized RegA is capable of binding to the ccoN promoter, which drives the expression of cytochrome cbb₃ oxidase subunits. This study provides a new model of aerobic regulation of gene expression by RegA involving the formation of an intermolecular disulfide bond. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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14 pages, 4009 KiB

Open AccessArticle

Structural Analyses of CrtJ and Its B₁₂-Binding Co-Regulators SAerR and LAerR from the Purple Photosynthetic Bacterium Rhodobacter capsulatus

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Vladimira Dragnea

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Giovanni Gonzalez-Gutierrez

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Carl E. Bauer

Microorganisms 2022, 10(5), 912; https://doi.org/10.3390/microorganisms10050912 - 27 Apr 2022

Cited by 1 | Viewed by 1353

Abstract

Among purple photosynthetic bacteria, the transcription factor CrtJ is a major regulator of photosystem gene expression. Depending on growing conditions, CrtJ can function as an aerobic repressor or an anaerobic activator of photosystem genes. Recently, CrtJ’s activity was shown to be modulated by [...] Read more.

Among purple photosynthetic bacteria, the transcription factor CrtJ is a major regulator of photosystem gene expression. Depending on growing conditions, CrtJ can function as an aerobic repressor or an anaerobic activator of photosystem genes. Recently, CrtJ’s activity was shown to be modulated by two size variants of a B₁₂ binding co-regulator called SAerR and LAerR in Rhodobacter capsulatus. The short form, SAerR, promotes CrtJ repression, while the longer variant, LAerR, converts CrtJ into an activator. In this study, we solved the crystal structure of R. capsulatus SAerR at a 2.25 Å resolution. Hydroxycobalamin bound to SAerR is sandwiched between a 4-helix bundle cap, and a Rossman fold. This structure is similar to a AerR-like domain present in CarH from Thermus termophilus, which is a combined photoreceptor/transcription regulator. We also utilized AlphaFold software to predict structures for the LAerR, CrtJ, SAerR-CrtJ and LAerR-CrtJ co-complexes. These structures provide insights into the role of B₁₂ and an LAerR N-terminal extension in regulating the activity of CrtJ. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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13 pages, 1650 KiB

Open AccessArticle

Persulfide-Responsive Transcription Factor SqrR Regulates Gene Transfer and Biofilm Formation via the Metabolic Modulation of Cyclic di-GMP in Rhodobacter capsulatus

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Microorganisms 2022, 10(5), 908; https://doi.org/10.3390/microorganisms10050908 - 26 Apr 2022

Cited by 3 | Viewed by 2180

Abstract

Bacterial phage-like particles (gene transfer agents—GTAs) are widely employed as a crucial genetic vector in horizontal gene transfer. GTA-mediated gene transfer is induced in response to various stresses; however, regulatory mechanisms are poorly understood. We found that the persulfide-responsive transcription factor SqrR may [...] Read more.

Bacterial phage-like particles (gene transfer agents—GTAs) are widely employed as a crucial genetic vector in horizontal gene transfer. GTA-mediated gene transfer is induced in response to various stresses; however, regulatory mechanisms are poorly understood. We found that the persulfide-responsive transcription factor SqrR may repress the expression of several GTA-related genes in the photosynthetic bacterium Rhodobacter capsulatus. Here, we show that the sqrR deletion mutant (ΔsqrR) produces higher amounts of intra- and extracellular GTA and gene transfer activity than the wild type (WT). The transcript levels of GTA-related genes are also increased in ΔsqrR. In spite of the presumption that GTA-related genes are regulated in response to sulfide by SqrR, treatment with sulfide did not alter the transcript levels of these genes in the WT strain. Surprisingly, hydrogen peroxide increased the transcript levels of GTA-related genes in the WT, and this alteration was abolished in the ΔsqrR strain. Moreover, the absence of SqrR changed the intracellular cyclic dimeric GMP (c-di-GMP) levels, and the amount of c-di-GMP was correlated with GTA activity and biofilm formation. These results suggest that SqrR is related to the repression of GTA production and the activation of biofilm formation via control of the intracellular c-di-GMP levels. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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12 pages, 2343 KiB

Open AccessArticle

Examination of Genetic Control Elements in the Phototrophic Firmicute Heliomicrobium modesticaldum

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Alexandria M. Layton

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Kevin E. Redding

Microorganisms 2022, 10(5), 876; https://doi.org/10.3390/microorganisms10050876 - 22 Apr 2022

Viewed by 1264

Abstract

Heliomicrobium modesticaldum has been used as a model organism for the Heliobacteria, the only phototrophic family in the Firmicutes. It is a moderately thermophilic anoxygenic phototrophic bacterium that is capable of fermentative growth in the dark. The genetic manipulation of H. modesticaldum is [...] Read more.

Heliomicrobium modesticaldum has been used as a model organism for the Heliobacteria, the only phototrophic family in the Firmicutes. It is a moderately thermophilic anoxygenic phototrophic bacterium that is capable of fermentative growth in the dark. The genetic manipulation of H. modesticaldum is still in its infancy. Methods to introduce genes through the use of exogenous plasmids and to delete genes from the chromosome through the use of the native CRISPR/Cas system have been developed in the last several years. To expand our genetic toolkit, it was necessary to control gene expression. In this study, we analyzed constitutive and inducible promoters developed for clostridia for their use in H. modesticaldum and further tested two reporters, adhB and lacZ, as indicators of promoter strength. Alcohol dehydrogenase (AdhB) was unsuitable as a reporter in this species due to high endogenous activity and/or low activity of the reporter, but a thermostable LacZ worked well as a reporter. A set of constitutive promoters previously reported to work in Clostridium thermocellum was found to be reliable for controlling the expression of the lacZ reporter gene in H. modesticaldum at a range of activities spanning an order of magnitude. An anhydrotetracycline-inducible promoter was created by inserting tetO operators into a strong constitutive promoter, but it was not fully repressible. The implementation of a xylose-inducible promoter resulted in complete repression of β-gal in the absence of xylose, and reliable expression tunable through the concentration of xylose added to the culture. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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18 pages, 1531 KiB

Open AccessArticle

Genomic Features of the Bundle-Forming Heliobacterium Heliophilum fasciatum

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Kelly S. Bender

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Michael T. Madigan

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Kyleigh L. Williamson

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Sophia A. Sanguedolce

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Abigail C. Brown

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W. Matthew Sattley

Microorganisms 2022, 10(5), 869; https://doi.org/10.3390/microorganisms10050869 - 21 Apr 2022

Cited by 1 | Viewed by 1404

Abstract

Eight species of heliobacteria have had their genomes sequenced. However, only two of these genomes have been analyzed in detail, those from the thermophilic Heliomicrobium (Hmi.) modesticaldum and the alkaliphilic Heliorestis (Hrs.) convoluta. Here we present analyses of the draft genome sequence [...] Read more.

Eight species of heliobacteria have had their genomes sequenced. However, only two of these genomes have been analyzed in detail, those from the thermophilic Heliomicrobium (Hmi.) modesticaldum and the alkaliphilic Heliorestis (Hrs.) convoluta. Here we present analyses of the draft genome sequence of a species of heliobacterium that grows optimally at a moderate temperature and neutral pH. The organism, Heliophilum (Hph.) fasciatum, is phylogenetically unique among cultured heliobacteria and was isolated from rice soil, a common habitat for heliobacteria. The Hph. fasciatum genome contains 3.14 Mbp—similar to that of other reported heliobacteria—but has a G+C base ratio that lies between that of Hmi. modesticaldum and Hrs. convoluta. Many of the genomic features of Hmi. modesticaldum and Hrs. convoluta, such as the absence of genes encoding autotrophic pathways, the presence of a superoperonal cluster of photosynthesis-related genes, and genes encoding endospore-specific proteins, are also characteristic of the Hph. fasciatum genome. However, despite the fact that Hph. fasciatum is diazotrophic, classical nif genes encoding the alpha and beta subunits of dinitrogenase (nifDK) present in other heliobacteria could not be identified. Instead, genes encoding several highly divergent NifDK homologs were present, at least one of which likely encodes a functional dinitrogenase and another a methylthio-alkane reductase (MarDK) for sulfur assimilation. A classical NifH (dinitrogenase reductase) homolog was also absent in Hph. fasciatum, but a related protein was identified that likely carries out this function as well as electron delivery to MarDK. The N₂-fixing system of Hph. fasciatum is therefore distinct from that of other heliobacteria and may have unusual properties. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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17 pages, 3781 KiB

Open AccessArticle

Cyclic Electron Flow-Coupled Proton Pumping in Synechocystis sp. PCC6803 Is Dependent upon NADPH Oxidation by the Soluble Isoform of Ferredoxin:NADP-Oxidoreductase

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Neil T. Miller

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Ghada Ajlani

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Robert L. Burnap

Microorganisms 2022, 10(5), 855; https://doi.org/10.3390/microorganisms10050855 - 21 Apr 2022

Cited by 1 | Viewed by 1706

Abstract

Ferredoxin:NADP-oxidoreductase (FNR) catalyzes the reversible exchange of electrons between ferredoxin (Fd) and NADP(H). Reduction of NADP⁺ by Fd via FNR is essential in the terminal steps of photosynthetic electron transfer, as light-activated electron flow produces NADPH for CO₂ assimilation. FNR also [...] Read more.

Ferredoxin:NADP-oxidoreductase (FNR) catalyzes the reversible exchange of electrons between ferredoxin (Fd) and NADP(H). Reduction of NADP⁺ by Fd via FNR is essential in the terminal steps of photosynthetic electron transfer, as light-activated electron flow produces NADPH for CO₂ assimilation. FNR also catalyzes the reverse reaction in photosynthetic organisms, transferring electrons from NADPH to Fd, which is important in cyanobacteria for respiration and cyclic electron flow (CEF). The cyanobacterium Synechocystis sp. PCC6803 possesses two isoforms of FNR, a large form attached to the phycobilisome (FNR_L) and a small form that is soluble (FNR_S). While both isoforms are capable of NADPH oxidation or NADP⁺ reduction, FNR_L is most abundant during typical growth conditions, whereas FNR_S accumulates under stressful conditions that require enhanced CEF. Because CEF-driven proton pumping in the light–dark transition is due to NDH-1 complex activity and they are powered by reduced Fd, CEF-driven proton pumping and the redox state of the PQ and NADP(H) pools were investigated in mutants possessing either FNR_L or FNR_S. We found that the FNR_S isoform facilitates proton pumping in the dark–light transition, contributing more to CEF than FNR_L. FNR_L is capable of providing reducing power for CEF-driven proton pumping, but only after an adaptation period to illumination. The results support that FNR_S is indeed associated with increased cyclic electron flow and proton pumping, which is consistent with the idea that stress conditions create a higher demand for ATP relative to NADPH. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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22 pages, 5152 KiB

Open AccessArticle

Discovery of Chlorophyll d: Isolation and Characterization of a Far-Red Cyanobacterium from the Original Site of Manning and Strain (1943) at Moss Beach, California

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Robert E. Blankenship

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Benjamin M. Wolf

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Angela M. Detweiler

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Kathy Ann Miller

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Jacob J. Schladweiler

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Ron Lindeman

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Mary N. Parenteau

Microorganisms 2022, 10(4), 819; https://doi.org/10.3390/microorganisms10040819 - 14 Apr 2022

Cited by 2 | Viewed by 2479

Abstract

We have isolated a chlorophyll-d-containing cyanobacterium from the intertidal field site at Moss Beach, on the coast of Central California, USA, where Manning and Strain (1943) originally discovered this far-red chlorophyll. Here, we present the cyanobacterium’s environmental description, culturing procedure, pigment [...] Read more.

We have isolated a chlorophyll-d-containing cyanobacterium from the intertidal field site at Moss Beach, on the coast of Central California, USA, where Manning and Strain (1943) originally discovered this far-red chlorophyll. Here, we present the cyanobacterium’s environmental description, culturing procedure, pigment composition, ultrastructure, and full genome sequence. Among cultures of far-red cyanobacteria obtained from red algae from the same site, this strain was an epiphyte on a brown macroalgae. Its Q_yin vivo absorbance peak is centered at 704–705 nm, the shortest wavelength observed thus far among the various known Acaryochloris strains. Its Chl a/Chl d ratio was 0.01, with Chl d accounting for 99% of the total Chl d and Chl a mass. TEM imagery indicates the absence of phycobilisomes, corroborated by both pigment spectra and genome analysis. The Moss Beach strain codes for only a single set of genes for producing allophycocyanin. Genomic sequencing yielded a 7.25 Mbp circular chromosome and 10 circular plasmids ranging from 16 kbp to 394 kbp. We have determined that this strain shares high similarity with strain S15, an epiphyte of red algae, while its distinct gene complement and ecological niche suggest that this strain could be the closest known relative to the original Chl d source of Manning and Strain (1943). The Moss Beach strain is designated Acaryochloris sp. (marina) strain Moss Beach. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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15 pages, 2858 KiB

Open AccessArticle

Comparative Genome Analysis of the Photosynthetic Betaproteobacteria of the Genus Rhodocyclus: Heterogeneity within Strains Assigned to Rhodocyclus tenuis and Description of Rhodocyclus gracilis sp. nov. as a New Species

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Microorganisms 2022, 10(3), 649; https://doi.org/10.3390/microorganisms10030649 - 18 Mar 2022

Cited by 5 | Viewed by 1806

Abstract

The genome sequences for Rhodocyclus purpureus DSM 168^T and four strains assigned to Rhodocyclus tenuis (DSM 110, DSM 111, DSM 112, and IM 230) have been determined. One of the strains studied (IM 230) has an average nucleotide identity (ANI) of 97% [...] Read more.

The genome sequences for Rhodocyclus purpureus DSM 168^T and four strains assigned to Rhodocyclus tenuis (DSM 110, DSM 111, DSM 112, and IM 230) have been determined. One of the strains studied (IM 230) has an average nucleotide identity (ANI) of 97% to the recently reported genome of the type strain DSM 109 of Rcy. tenuis and is regarded as virtually identical at the species level. The ANI of 80% for three other strains (DSM 110, DSM 111, DSM 112) to the type strain of Rcy. tenuis points to a differentiation of these at the species level. Rcy. purpureus is equidistant from Rcy. tenuis and the new species, based on both ANI (78–80%) and complete proteome comparisons (70% AAI). Strains DSM 110, DSM 111, and DSM 112 are very closely related to each other based on ANI, whole genome, and proteome comparisons but clearly distinct from the Rcy. tenuis type strain DSM 109. In addition to the whole genome differentiation, these three strains also contain unique genetic differences in cytochrome genes and contain genes for an anaerobic cobalamin synthesis pathway that is lacking from both Rcy. tenuis and Rcy. purpureus. Based on genomic and genetic differences, these three strains should be considered to represent a new species, which is distinctly different from both Rcy. purpureus and Rcy. tenuis, for which the new name Rhodocyclus gracilis sp. nov. is proposed. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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16 pages, 2401 KiB

Open AccessArticle

Genomic and Functional Variation of the Chlorophyll d-Producing Cyanobacterium Acaryochloris marina

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Scott R. Miller

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Heidi E. Abresch

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Jacob J. Baroch

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Caleb K. Fishman Miller

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Arkadiy I. Garber

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Andrew R. Oman

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Nikea J. Ulrich

Microorganisms 2022, 10(3), 569; https://doi.org/10.3390/microorganisms10030569 - 06 Mar 2022

Cited by 2 | Viewed by 1827

Abstract

The Chlorophyll d-producing cyanobacterium Acaryochloris marina is widely distributed in marine environments enriched in far-red light, but our understanding of its genomic and functional diversity is limited. Here, we take an integrative approach to investigate A. marina diversity for 37 strains, which [...] Read more.

The Chlorophyll d-producing cyanobacterium Acaryochloris marina is widely distributed in marine environments enriched in far-red light, but our understanding of its genomic and functional diversity is limited. Here, we take an integrative approach to investigate A. marina diversity for 37 strains, which includes twelve newly isolated strains from previously unsampled locations in Europe and the Pacific Northwest of North America. A genome-wide phylogeny revealed both that closely related A. marina have migrated within geographic regions and that distantly related A. marina lineages can co-occur. The distribution of traits mapped onto the phylogeny provided evidence of a dynamic evolutionary history of gene gain and loss during A. marina diversification. Ancestral genes that were differentially retained or lost by strains include plasmid-encoded sodium-transporting ATPase and bidirectional NiFe-hydrogenase genes that may be involved in salt tolerance and redox balance under fermentative conditions, respectively. The acquisition of genes by horizontal transfer has also played an important role in the evolution of new functions, such as nitrogen fixation. Together, our results resolve examples in which genome content and ecotypic variation for nutrient metabolism and environmental tolerance have diversified during the evolutionary history of this unusual photosynthetic bacterium. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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7 pages, 625 KiB

Open AccessCommunication

Expression of Scytonemin Biosynthesis Genes under Alternative Stress Conditions in the Cyanobacterium Nostoc punctiforme

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Janine Bennett

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Tanya Soule

Microorganisms 2022, 10(2), 427; https://doi.org/10.3390/microorganisms10020427 - 12 Feb 2022

Cited by 4 | Viewed by 1620

Abstract

The indole-alkaloid scytonemin is a sunscreen pigment that is widely produced among cyanobacteria as an ultraviolet radiation (UVR) survival strategy. Scytonemin biosynthesis is encoded by two gene clusters that are known to be induced by long-wavelength radiation (UVA). Previous studies have characterized the [...] Read more.

The indole-alkaloid scytonemin is a sunscreen pigment that is widely produced among cyanobacteria as an ultraviolet radiation (UVR) survival strategy. Scytonemin biosynthesis is encoded by two gene clusters that are known to be induced by long-wavelength radiation (UVA). Previous studies have characterized the transcriptome of cyanobacteria in response to a wide range of conditions, but the effect on the expression of scytonemin biosynthesis genes has not been specifically targeted. Therefore, the aim of this study is to determine the variable response of scytonemin biosynthesis genes to a variety of environmental conditions. Cells were acclimated to white light before supplementation with UVA, UVB, high light, or osmotic stress for 48 h. The presence of scytonemin was determined by absorbance spectroscopy and gene expression of representative scytonemin biosynthesis genes was measured using quantitative PCR. Scytonemin genes were up-regulated in UVA, UVB, and high light, although the scytonemin pigment was not detected under high light. There was no scytonemin or upregulation of these genes under osmotic stress. The lack of pigment production under high light, despite increased gene expression, suggests a time-dependent delay for pigment production or additional mechanisms or genes that may be involved in scytonemin production beyond those currently known. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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22 pages, 4471 KiB

Open AccessArticle

Genomic Comparison, Phylogeny and Taxonomic Reevaluation of the Ectothiorhodospiraceae and Description of Halorhodospiraceae fam. nov. and Halochlorospira gen. nov.

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Johannes F. Imhoff

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John A. Kyndt

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Terrance E. Meyer

Microorganisms 2022, 10(2), 295; https://doi.org/10.3390/microorganisms10020295 - 26 Jan 2022

Cited by 7 | Viewed by 2655

Abstract

The Ectothiorhodospiraceae family represents purple sulfur bacteria of the Gammaproteobacteria found primarily in alkaline soda lakes of moderate to extremely high salinity. The main microscopically visible characteristic separating them from the Chromatiaceae is the excretion of the intermediate elemental sulfur formed during oxidation [...] Read more.

The Ectothiorhodospiraceae family represents purple sulfur bacteria of the Gammaproteobacteria found primarily in alkaline soda lakes of moderate to extremely high salinity. The main microscopically visible characteristic separating them from the Chromatiaceae is the excretion of the intermediate elemental sulfur formed during oxidation of sulfide prior to complete oxidation to sulfate rather than storing it in the periplasm. We present a comparative study of 38 genomes of all species of phototrophic Ectothiorhodospiraceae. We also include a comparison with those chemotrophic bacteria that have been assigned to the family previously and critically reevaluate this assignment. The data demonstrate the separation of Halorhodospira species in a major phylogenetic branch distant from other Ectothiorhodospiraceae and support their separation into a new family, for which the name Halorhodospiraceae fam. nov. is proposed. In addition, the green-colored, bacteriochlorophyll-containing species Halorhodospira halochloris and Halorhodospira abdelmalekii were transferred to the new genus Halochlorospira gen. nov. of this family. The data also enable classification of several so far unclassified isolates and support the separation of Ectothiorhodospira shaposhnikovii and Ect. vacuolata as well as Ect. mobilis and Ect. marismortui as distinct species. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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17 pages, 2273 KiB

Open AccessArticle

Host Cyanobacteria Killing by Novel Lytic Cyanophage YongM: A Protein Profiling Analysis

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Microorganisms 2022, 10(2), 257; https://doi.org/10.3390/microorganisms10020257 - 24 Jan 2022

Cited by 4 | Viewed by 2818

Abstract

Cyanobacteria are autotrophic prokaryotes that can proliferate robustly in eutrophic waters through photosynthesis. This can lead to outbreaks of lake “water blooms”, which result in water quality reduction and environmental pollution that seriously affect fisheries and aquaculture. The use of cyanophages to control [...] Read more.

Cyanobacteria are autotrophic prokaryotes that can proliferate robustly in eutrophic waters through photosynthesis. This can lead to outbreaks of lake “water blooms”, which result in water quality reduction and environmental pollution that seriously affect fisheries and aquaculture. The use of cyanophages to control the growth of cyanobacteria is an important strategy to tackle annual cyanobacterial blooms. YongM is a novel lytic cyanophage with a broad host spectrum and high efficiency in killing its host, cyanobacteria FACHB-596. However, changes in cyanophage protein profile during infestation and killing of the host remains unknown. To characterize the proteins and its regulation networks involved in the killing of host cyanobacteria by YongM and evaluate whether this strain YongM could be used as a chassis for further engineering to be a powerful tool in dealing with cyanobacterial blooms, we herein applied 4D label-free high-throughput quantitative proteomics to analyze differentially expressed proteins (DEPs) involved in cyanobacteria host response infected 1 and 8 h with YongM cyanophage. Metabolic pathways, such as photosynthesis, photosynthesis-antennal protein, oxidative phosphorylation, ribosome, carbon fixation, and glycolysis/glycol-isomerization were significantly altered in the infested host, whereas DEPs were associated with the metabolic processes of photosynthesis, precursor metabolites, energy production, and organic nitrogen compounds. Among these DEPs, key proteins involved in YongM-host interaction may be photosystem I P700 chlorophyll-a apolipoprotein, carbon dioxide concentration mechanism protein, cytochrome B, and some YongM infection lysis-related enzymes. Our results provide comprehensive information of protein profiles during the invasion and killing of host cyanobacteria by its cyanophage, which may shed light on future design and manipulation of artificial cyanophages against water blooms. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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18 pages, 2475 KiB

Open AccessArticle

Elioraea tepida, sp. nov., a Moderately Thermophilic Aerobic Anoxygenic Phototrophic Bacterium Isolated from the Mat Community of an Alkaline Siliceous Hot Spring in Yellowstone National Park, WY, USA

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Microorganisms 2022, 10(1), 80; https://doi.org/10.3390/microorganisms10010080 - 31 Dec 2021

Cited by 1 | Viewed by 2001

Abstract

Strain MS-P2^T was isolated from microbial mats associated with Mushroom Spring, an alkaline siliceous hot spring in Yellowstone National Park, WY, USA. The isolate grows chemoheterotrophically by oxygen-dependent respiration, and light stimulates photoheterotrophic growth under strictly oxic conditions. Strain MS-P2^T synthesizes [...] Read more.

Strain MS-P2^T was isolated from microbial mats associated with Mushroom Spring, an alkaline siliceous hot spring in Yellowstone National Park, WY, USA. The isolate grows chemoheterotrophically by oxygen-dependent respiration, and light stimulates photoheterotrophic growth under strictly oxic conditions. Strain MS-P2^T synthesizes bacteriochlorophyll a and the carotenoid spirilloxanthin. However, photoautotrophic growth did not occur under oxic or anoxic conditions, suggesting that this strain should be classified as an aerobic anoxygenic phototrophic bacterium. Strain MS-P2^T cells are motile, curved rods about 0.5 to 1.0 μm wide and 1.0 to 1.5 μm long. The optimum growth temperature is 45–50 °C, and the optimum pH for growth is circum-neutral (pH 7.0–7.5). Sequence analysis of the 16S rRNA gene revealed that strain MS-P2^T is closely related to Elioraea species, members of the class Alphaproteobacteria, with a sequence identity of 96.58 to 98%. The genome of strain MS-P2^T is a single circular DNA molecule of 3,367,643 bp with a mol% guanine-plus-cytosine content of 70.6%. Based on phylogenetic, physiological, biochemical, and genomic characteristics, we propose this bacteriochlorophyll a-containing isolate is a new species belonging to the genus Elioraea, with the suggested name Elioraeatepida. The type-strain is strain MS-P2^T (= JCM33060^T = ATCC TSD-174^T). Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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19 pages, 1090 KiB

Open AccessReview

Advances in the Understanding of the Lifecycle of Photosystem II

by

Virginia M. Johnson

and

Himadri B. Pakrasi

Microorganisms 2022, 10(5), 836; https://doi.org/10.3390/microorganisms10050836 - 19 Apr 2022

Cited by 6 | Viewed by 2866

Abstract

Photosystem II is a light-driven water-plastoquinone oxidoreductase present in cyanobacteria, algae and plants. It produces molecular oxygen and protons to drive ATP synthesis, fueling life on Earth. As a multi-subunit membrane-protein-pigment complex, Photosystem II undergoes a dynamic cycle of synthesis, damage, and repair [...] Read more.

Photosystem II is a light-driven water-plastoquinone oxidoreductase present in cyanobacteria, algae and plants. It produces molecular oxygen and protons to drive ATP synthesis, fueling life on Earth. As a multi-subunit membrane-protein-pigment complex, Photosystem II undergoes a dynamic cycle of synthesis, damage, and repair known as the Photosystem II lifecycle, to maintain a high level of photosynthetic activity at the cellular level. Cyanobacteria, oxygenic photosynthetic bacteria, are frequently used as model organisms to study oxygenic photosynthetic processes due to their ease of growth and genetic manipulation. The cyanobacterial PSII structure and function have been well-characterized, but its lifecycle is under active investigation. In this review, advances in studying the lifecycle of Photosystem II in cyanobacteria will be discussed, with a particular emphasis on new structural findings enabled by cryo-electron microscopy. These structural findings complement a rich and growing body of biochemical and molecular biology research into Photosystem II assembly and repair. Full article

(This article belongs to the Special Issue Phototrophic Bacteria)

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