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Microbial One-Carbon Metabolism of Natural and Engineered Systems

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (31 March 2021) | Viewed by 36857

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Dr. Françoise Bringel

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CNRS Génétique Moléculaire, Génomique, Microbiologie, Université de Strasbourg, UMR 7156 UNISTRA-CNRS, 28 rue Goethe, 67083 Strasbourg, France
Interests: functional and comparative genomics of microbial one-carbon compound metabolism

Dr. Emilie Muller

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CNRS Génétique Moléculaire, Génomique, Microbiologie, Université de Strasbourg, UMR 7156 UNISTRA-CNRS, 28 rue Goethe, 67083 Strasbourg, France
Interests: microbial ecology and lifestyle strategy

Prof. Dr. Stéphane Vuilleumier

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CNRS Génétique Moléculaire, Génomique, Microbiologie, Université de Strasbourg, UMR 7156 UNISTRA-CNRS, 28 rue Goethe, 67083 Strasbourg, France
Interests: microbial one-carbon compound metabolism

Special Issue Information

Dear Colleagues,

The goal of this Special Issue will be to provide a broad overview of the recent breakthroughs and current questions in the dynamic field of microbial C1 metabolism, as a crucial component of the biogeochemical processes of the planet in the Anthropocene. Contributions will range from the molecular level of model systems, to the global scale of environmental ecosystems, biogeochemical cycles, and natural and engineered ecosystems. The Special Issue will present fundamental and applied research on microorganisms, both cultured and uncultured, that are able to use C1 compounds, and compounds lacking carbon–carbon bonds for growth, including, for example, autotrophs, methylotrophs, phototrophs, methanogens, and acetogens. Topics will cover the physiology, genetics, ecology, and evolution of the microbial C1 metabolism in emblematic environments and ecosystems, corresponding to processes of chemical and light energy conversion, key enzymes of microbial C1 metabolism, and biotechnological applications in the context of the ongoing massive global change.

Dr. Françoise Bringel
Dr. Emilie Muller
Prof. Dr. Stéphane Vuilleumier
Guest Editors

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Keywords

carbon cycling
one-carbon metabolism
microbial ecology
synthetic biology

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Microbial C1 Metabolism in Microorganisms (10 articles)

Published Papers (10 papers)

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Research

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12 pages, 1577 KiB

Open AccessArticle

Genome-Wide Transcription Start Sites Mapping in Methylorubrum Grown with Dichloromethane and Methanol

by Bruno Maucourt, David Roche, Pauline Chaignaud, Stéphane Vuilleumier and Françoise Bringel

Microorganisms 2022, 10(7), 1301; https://doi.org/10.3390/microorganisms10071301 - 27 Jun 2022

Viewed by 1784

Abstract

Dichloromethane (DCM, methylene chloride) is a toxic halogenated volatile organic compound massively used for industrial applications, and consequently often detected in the environment as a major pollutant. DCM biotransformation suggests a sustainable decontamination strategy of polluted sites. Among methylotrophic bacteria able to use DCM as a sole source of carbon and energy for growth, Methylorubrum extorquens DM4 is a longstanding reference strain. Here, the primary 5′-ends of transcripts were obtained using a differential RNA-seq (dRNA-seq) approach to provide the first transcription start site (TSS) genome-wide landscape of a methylotroph using DCM or methanol. In total, 7231 putative TSSs were annotated and classified with respect to their localization to coding sequences (CDSs). TSSs on the opposite strand of CDS (antisense TSS) account for 31% of all identified TSSs. One-third of the detected TSSs were located at a distance to the start codon inferior to 250 nt (average of 84 nt) with 7% of leaderless mRNA. Taken together, the global TSS map for bacterial growth using DCM or methanol will facilitate future studies in which transcriptional regulation is crucial, and efficient DCM removal at polluted sites is limited by regulatory processes. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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15 pages, 769 KiB

Open AccessEditor’s ChoiceArticle

The Autotrophic Core: An Ancient Network of 404 Reactions Converts H₂, CO₂, and NH₃ into Amino Acids, Bases, and Cofactors

by Jessica L. E. Wimmer, Andrey do Nascimento Vieira, Joana C. Xavier, Karl Kleinermanns, William F. Martin and Martina Preiner

Microorganisms 2021, 9(2), 458; https://doi.org/10.3390/microorganisms9020458 - 23 Feb 2021

Cited by 18 | Viewed by 6223

Abstract

The metabolism of cells contains evidence reflecting the process by which they arose. Here, we have identified the ancient core of autotrophic metabolism encompassing 404 reactions that comprise the reaction network from H₂, CO₂, and ammonia (NH₃) to amino acids, nucleic acid monomers, and the 19 cofactors required for their synthesis. Water is the most common reactant in the autotrophic core, indicating that the core arose in an aqueous environment. Seventy-seven core reactions involve the hydrolysis of high-energy phosphate bonds, furthermore suggesting the presence of a non-enzymatic and highly exergonic chemical reaction capable of continuously synthesizing activated phosphate bonds. CO₂ is the most common carbon-containing compound in the core. An abundance of NADH and NADPH-dependent redox reactions in the autotrophic core, the central role of CO₂, and the circumstance that the core’s main products are far more reduced than CO₂ indicate that the core arose in a highly reducing environment. The chemical reactions of the autotrophic core suggest that it arose from H₂, inorganic carbon, and NH₃ in an aqueous environment marked by highly reducing and continuously far from equilibrium conditions. Such conditions are very similar to those found in serpentinizing hydrothermal systems. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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22 pages, 3776 KiB

Open AccessArticle

Global Transcriptional Response of Methylorubrum extorquens to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition

by Jannell V. Bazurto, Siavash Riazi, Simon D’Alton, Daniel E. Deatherage, Eric L. Bruger, Jeffrey E. Barrick and Christopher J. Marx

Microorganisms 2021, 9(2), 347; https://doi.org/10.3390/microorganisms9020347 - 10 Feb 2021

Cited by 4 | Viewed by 3198

Abstract

The potency and indiscriminate nature of formaldehyde reactivity upon biological molecules make it a universal stressor. However, some organisms such as Methylorubrum extorquens possess means to rapidly and effectively mitigate formaldehyde-induced damage. EfgA is a recently identified formaldehyde sensor predicted to halt translation in response to elevated formaldehyde as a means to protect cells. Herein, we investigate growth and changes in gene expression to understand how M. extorquens responds to formaldehyde with and without the EfgA-formaldehyde-mediated translational response, and how this mechanism compares to antibiotic-mediated translation inhibition. These distinct mechanisms of translation inhibition have notable differences: they each involve different specific players and in addition, formaldehyde also acts as a general, multi-target stressor and a potential carbon source. We present findings demonstrating that in addition to its characterized impact on translation, functional EfgA allows for a rapid and robust transcriptional response to formaldehyde and that removal of EfgA leads to heightened proteotoxic and genotoxic stress in the presence of increased formaldehyde levels. We also found that many downstream consequences of translation inhibition were shared by EfgA-formaldehyde- and kanamycin-mediated translation inhibition. Our work uncovered additional layers of regulatory control enacted by functional EfgA upon experiencing formaldehyde stress, and further demonstrated the importance this protein plays at both transcriptional and translational levels in this model methylotroph. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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20 pages, 32799 KiB

Open AccessArticle

Cross-Feeding of a Toxic Metabolite in a Synthetic Lignocellulose-Degrading Microbial Community

by Jessica A. Lee, Alyssa C. Baugh, Nicholas J. Shevalier, Brandi Strand, Sergey Stolyar and Christopher J. Marx

Microorganisms 2021, 9(2), 321; https://doi.org/10.3390/microorganisms9020321 - 04 Feb 2021

Cited by 8 | Viewed by 3194

Abstract

The recalcitrance of complex organic polymers such as lignocellulose is one of the major obstacles to sustainable energy production from plant biomass, and the generation of toxic intermediates can negatively impact the efficiency of microbial lignocellulose degradation. Here, we describe the development of a model microbial consortium for studying lignocellulose degradation, with the specific goal of mitigating the production of the toxin formaldehyde during the breakdown of methoxylated aromatic compounds. Included are Pseudomonas putida, a lignin degrader; Cellulomonas fimi, a cellulose degrader; and sometimes Yarrowia lipolytica, an oleaginous yeast. Unique to our system is the inclusion of Methylorubrum extorquens, a methylotroph capable of using formaldehyde for growth. We developed a defined minimal “Model Lignocellulose” growth medium for reproducible coculture experiments. We demonstrated that the formaldehyde produced by P. putida growing on vanillic acid can exceed the minimum inhibitory concentration for C. fimi, and, furthermore, that the presence of M. extorquens lowers those concentrations. We also uncovered unexpected ecological dynamics, including resource competition, and interspecies differences in growth requirements and toxin sensitivities. Finally, we introduced the possibility for a mutualistic interaction between C. fimi and M. extorquens through metabolite exchange. This study lays the foundation to enable future work incorporating metabolomic analysis and modeling, genetic engineering, and laboratory evolution, on a model system that is appropriate both for fundamental eco-evolutionary studies and for the optimization of efficiency and yield in microbially-mediated biomass transformation. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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12 pages, 2617 KiB

Open AccessArticle

Energy Conservation in the Acetogenic Bacterium Clostridium aceticum

by Anja Wiechmann and Volker Müller

Microorganisms 2021, 9(2), 258; https://doi.org/10.3390/microorganisms9020258 - 27 Jan 2021

Cited by 7 | Viewed by 2549

Abstract

In times of global warming caused by the extensive use of fossil fuels, the need to capture gaseous carbon compounds is growing bigger. Several groups of microorganisms can fix the greenhouse gas CO₂. Out of these, acetogenic bacteria are role models in their ability to reduce CO₂ with hydrogen to acetate, which makes acetogens prime candidates for genetic modification towards biotechnological production of value-added compounds from CO₂, such as biofuels. However, growth of acetogens on gaseous substrates is strongly energy-limited, and successful metabolic engineering requires a detailed knowledge of the bioenergetics. In 1939, Clostridium aceticum was the first acetogen to be described. A recent genomic study revealed that this organism contains cytochromes and therefore may use a proton gradient in its respiratory chain. We have followed up these studies and will present data that C. aceticum does not use a H⁺ but a Na⁺ gradient for ATP synthesis, established by a Na⁺-Rnf. Experimental data and in silico analyses enabled us to propose the biochemistry and bioenergetics of acetogenesis from H₂ + CO₂ in C. aceticum. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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16 pages, 2616 KiB

Open AccessArticle

Dichloromethane Degradation Pathway from Unsequenced Hyphomicrobium sp. MC8b Rapidly Explored by Pan-Proteomics

by Karim Hayoun, Emilie Geersens, Cédric C. Laczny, Rashi Halder, Carmen Lázaro Sánchez, Abhijit Manna, Françoise Bringel, Michaël Ryckelynck, Paul Wilmes, Emilie E. L. Muller, Béatrice Alpha-Bazin, Jean Armengaud and Stéphane Vuilleumier

Microorganisms 2020, 8(12), 1876; https://doi.org/10.3390/microorganisms8121876 - 27 Nov 2020

Cited by 5 | Viewed by 2576

Abstract

Several bacteria are able to degrade the major industrial solvent dichloromethane (DCM) by using the conserved dehalogenase DcmA, the only system for DCM degradation characterised at the sequence level so far. Using differential proteomics, we rapidly identified key determinants of DCM degradation for Hyphomicrobium sp. MC8b, an unsequenced facultative methylotrophic DCM-degrading strain. For this, we designed a pan-proteomics database comprising the annotated genome sequences of 13 distinct Hyphomicrobium strains. Compared to growth with methanol, growth with DCM induces drastic changes in the proteome of strain MC8b. Dichloromethane dehalogenase DcmA was detected by differential pan-proteomics, but only with poor sequence coverage, suggesting atypical characteristics of the DCM dehalogenation system in this strain. More peptides were assigned to DcmA by error-tolerant search, warranting subsequent sequencing of the genome of strain MC8b, which revealed a highly divergent set of dcm genes in this strain. This suggests that the dcm enzymatic system is less strongly conserved than previously believed, and that substantial molecular evolution of dcm genes has occurred beyond their horizontal transfer in the bacterial domain. Our study showed the power of pan-proteomics for quick characterization of new strains belonging to branches of the Tree of Life that are densely genome-sequenced. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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17 pages, 4861 KiB

Open AccessArticle

Lanthanide-Dependent Methanol and Formaldehyde Oxidation in Methylobacterium aquaticum Strain 22A

by Patcha Yanpirat, Yukari Nakatsuji, Shota Hiraga, Yoshiko Fujitani, Terumi Izumi, Sachiko Masuda, Ryoji Mitsui, Tomoyuki Nakagawa and Akio Tani

Microorganisms 2020, 8(6), 822; https://doi.org/10.3390/microorganisms8060822 - 30 May 2020

Cited by 14 | Viewed by 4031

Abstract

Lanthanides (Ln) are an essential cofactor for XoxF-type methanol dehydrogenases (MDHs) in Gram-negative methylotrophs. The Ln³⁺ dependency of XoxF has expanded knowledge and raised new questions in methylotrophy, including the differences in characteristics of XoxF-type MDHs, their regulation, and the methylotrophic metabolism including formaldehyde oxidation. In this study, we genetically identified one set of Ln³⁺- and Ca²⁺-dependent MDHs (XoxF1 and MxaFI), that are involved in methylotrophy, and an ExaF-type Ln³⁺-dependent ethanol dehydrogenase, among six MDH-like genes in Methylobacterium aquaticum strain 22A. We also identified the causative mutations in MxbD, a sensor kinase necessary for mxaF expression and xoxF1 repression, for suppressive phenotypes in xoxF1 mutants defective in methanol growth even in the absence of Ln³⁺. Furthermore, we examined the phenotypes of a series of formaldehyde oxidation-pathway mutants (fae1, fae2, mch in the tetrahydromethanopterin (H₄MPT) pathway and hgd in the glutathione-dependent formaldehyde dehydrogenase (GSH) pathway). We found that MxaF produces formaldehyde to a toxic level in the absence of the formaldehyde oxidation pathways and that either XoxF1 or ExaF can oxidize formaldehyde to alleviate formaldehyde toxicity in vivo. Furthermore, the GSH pathway has a supportive role for the net formaldehyde oxidation in addition to the H₄MPT pathway that has primary importance. Studies on methylotrophy in Methylobacterium species have a long history, and this study provides further insights into genetic and physiological diversity and the differences in methylotrophy within the plant-colonizing methylotrophs. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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17 pages, 2514 KiB

Open AccessArticle

Metagenomic- and Cultivation-Based Exploration of Anaerobic Chloroform Biotransformation in Hypersaline Sediments as Natural Source of Chloromethanes

by Peng Peng, Yue Lu, Tom N.P. Bosma, Ivonne Nijenhuis, Bart Nijsse, Sudarshan A. Shetty, Alexander Ruecker, Alexander Umanets, Javier Ramiro-Garcia, Andreas Kappler, Detmer Sipkema, Hauke Smidt and Siavash Atashgahi

Microorganisms 2020, 8(5), 665; https://doi.org/10.3390/microorganisms8050665 - 02 May 2020

Cited by 7 | Viewed by 3838

Abstract

Chloroform (CF) is an environmental contaminant that can be naturally formed in various environments ranging from forest soils to salt lakes. Here we investigated CF removal potential in sediments obtained from hypersaline lakes in Western Australia. Reductive dechlorination of CF to dichloromethane (DCM) was observed in enrichment cultures derived from sediments of Lake Strawbridge, which has been reported as a natural source of CF. No CF removal was observed in abiotic control cultures without artificial electron donors, indicating biotic CF dechlorination in the enrichment cultures. Increasing vitamin B₁₂ concentration from 0.04 to 4 µM in enrichment cultures enhanced CF removal and reduced DCM formation. In cultures amended with 4 µM vitamin B₁₂ and ¹³C labelled CF, formation of ¹³CO₂ was detected. Known organohalide-respiring bacteria and reductive dehalogenase genes were neither detected using quantitative PCR nor metagenomic analysis of the enrichment cultures. Rather, members of the order Clostridiales, known to co-metabolically transform CF to DCM and CO₂, were detected. Accordingly, metagenome-assembled genomes of Clostridiales encoded enzymatic repertoires for the Wood-Ljungdahl pathway and cobalamin biosynthesis, which are known to be involved in fortuitous and nonspecific CF transformation. This study indicates that hypersaline lake microbiomes may act as a filter to reduce CF emission to the atmosphere. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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15 pages, 2034 KiB

Open AccessArticle

Microbial Community Structure and Methane Cycling Potential along a Thermokarst Pond-Peatland Continuum

by Adrien Vigneron, Perrine Cruaud, Najat Bhiry, Connie Lovejoy and Warwick F. Vincent

Microorganisms 2019, 7(11), 486; https://doi.org/10.3390/microorganisms7110486 - 24 Oct 2019

Cited by 14 | Viewed by 3790

Abstract

The thawing of ice-rich permafrost soils in northern peatlands leads to the formation of thermokarst ponds, surrounded by organic-rich soils. These aquatic ecosystems are sites of intense microbial activity, and CO₂ and CH₄ emissions. Many of the pond systems in northern landscapes and their surrounding peatlands are hydrologically contiguous, but little is known about the microbial connectivity of concentric habitats around the thermokarst ponds, or the effects of peat accumulation and infilling on the microbial communities. Here we investigated microbial community structure and abundance in a thermokarst pond-peatland system in subarctic Canada. Several lineages were ubiquitous, supporting a prokaryotic continuum from the thermokarst pond to surrounding peatlands. However, the microbial community structure shifted from typical aerobic freshwater microorganisms (Betaproteobacteria and Alphaproteobacteria) in the pond towards acidophilic and anaerobic lineages (Acidobacteria and Choroflexi) in the connected peatland waters, likely selected by the acidification of the water by Sphagnum mosses. Marked changes in abundance and community composition of methane cycling microorganisms were detected along the thermokarst pond-peatland transects, suggesting fine tuning of C-1 carbon cycling within a highly connected system, and warranting the need for higher spatial resolution across the thermokarst landscape to accurately predict net greenhouse gas emissions from northern peatlands. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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11 pages, 1733 KiB

Open AccessReview

Physiology of Methylotrophs Living in the Phyllosphere

by Hiroya Yurimoto, Kosuke Shiraishi and Yasuyoshi Sakai

Microorganisms 2021, 9(4), 809; https://doi.org/10.3390/microorganisms9040809 - 12 Apr 2021

Cited by 17 | Viewed by 4703

Abstract

Methanol is abundant in the phyllosphere, the surface of the above-ground parts of plants, and its concentration oscillates diurnally. The phyllosphere is one of the major habitats for a group of microorganisms, the so-called methylotrophs, that utilize one-carbon (C1) compounds, such as methanol and methane, as their sole source of carbon and energy. Among phyllospheric microorganisms, methanol-utilizing methylotrophic bacteria, known as pink-pigmented facultative methylotrophs (PPFMs), are the dominant colonizers of the phyllosphere, and some of them have recently been shown to have the ability to promote plant growth and increase crop yield. In addition to PPFMs, methanol-utilizing yeasts can proliferate and survive in the phyllosphere by using unique molecular and cellular mechanisms to adapt to the stressful phyllosphere environment. This review describes our current understanding of the physiology of methylotrophic bacteria and yeasts living in the phyllosphere where they are exposed to diurnal cycles of environmental conditions. Full article

(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)

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