Myxobacteria: Physiology and Regulation

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

Deadline for manuscript submissions: closed (31 October 2021) | Viewed by 26268

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Special Issue Editor

Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Ceredigion SY23 3DD, UK
Interests: myxobacteria
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Myxobacteria are fascinating prokaryotes. Their genomes are exceptionally large, endowing them with a wide range of interesting behaviors, including (but certainly not limited to) multicellular fruiting body formation, gliding motility, social interactions, predation, and secondary metabolite production. Their ecological importance in major ecosystems is becoming established, and we are beginning to understand the evolutionary forces that have shaped their current phenotypes and behaviors. Novel species of myxobacteria are steadily being discovered, often producing unusual metabolites and enzymes. There is also significant biotechnological interest in these organisms for a huge range of potential applications. Molecular studies, ranging in subject from individual enzymes to entire ‘omes, continue to provide rich insights into myxobacterial biology.

This Special Issue seeks to bring together a snapshot of current myxobacterial research, in all its diversity. It welcomes both original research articles as well as reviews, and when completed will be a primer for researchers who are not familiar with the myxobacteria and a resource for those already in the field. The remit of this Special Issue is therefore deliberately broad, and includes any aspect of myxobacterial biology. It is a pleasure to invite authors to submit their original research or review articles to the Special Issue.

Dr. David Whitworth
Guest Editor

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Keywords

  • ecology
  • evolution
  • fruiting body formation
  • genetics
  • metabolism
  • motility
  • ‘omes
  • predation
  • secondary metabolites
  • signaling
  • sporulation

Published Papers (9 papers)

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Editorial

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2 pages, 164 KiB  
Editorial
Myxobacteria: Physiology and Regulation
Microorganisms 2022, 10(4), 805; https://doi.org/10.3390/microorganisms10040805 - 12 Apr 2022
Cited by 2 | Viewed by 1397
Abstract
Myxobacteria are fascinating and important prokaryotes [...] Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)

Research

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14 pages, 1077 KiB  
Article
Predatory Bacteria Select for Sustained Prey Diversity
Microorganisms 2021, 9(10), 2079; https://doi.org/10.3390/microorganisms9102079 - 02 Oct 2021
Cited by 3 | Viewed by 2250
Abstract
Predator impacts on prey diversity are often studied among higher organisms over short periods, but microbial predator-prey systems allow examination of prey-diversity dynamics over evolutionary timescales. We previously showed that Escherichia coli commonly evolved minority mucoid phenotypes in response to predation by the [...] Read more.
Predator impacts on prey diversity are often studied among higher organisms over short periods, but microbial predator-prey systems allow examination of prey-diversity dynamics over evolutionary timescales. We previously showed that Escherichia coli commonly evolved minority mucoid phenotypes in response to predation by the bacterial predator Myxococcus xanthus by one time point of a coevolution experiment now named MyxoEE-6. Here we examine mucoid frequencies across several MyxoEE-6 timepoints to discriminate between the hypotheses that mucoids were increasing to fixation, stabilizing around equilibrium frequencies, or heading to loss toward the end of MyxoEE-6. In four focal coevolved prey populations, mucoids rose rapidly early in the experiment and then fluctuated within detectable minority frequency ranges through the end of MyxoEE-6, generating frequency dynamics suggestive of negative frequency-dependent selection. However, a competition experiment between mucoid and non-mucoid clones found a predation-specific advantage of the mucoid clone that was insensitive to frequency over the examined range, leaving the mechanism that maintains minority mucoidy unresolved. The advantage of mucoidy under predation was found to be associated with reduced population size after growth (productivity) in the absence of predators, suggesting a tradeoff between productivity and resistance to predation that we hypothesize may reverse mucoid vs non-mucoid fitness ranks within each MyxoEE-6 cycle. We also found that mucoidy was associated with diverse colony phenotypes and diverse candidate mutations primarily localized in the exopolysaccharide operon yjbEFGH. Collectively, our results show that selection from predatory bacteria can generate apparently stable sympatric phenotypic polymorphisms within coevolving prey populations and also allopatric diversity across populations by selecting for diverse mutations and colony phenotypes associated with mucoidy. More broadly, our results suggest that myxobacterial predation increases long-term diversity within natural microbial communities. Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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19 pages, 3991 KiB  
Article
Quantification of Myxococcus xanthus Aggregation and Rippling Behaviors: Deep-Learning Transformation of Phase-Contrast into Fluorescence Microscopy Images
Microorganisms 2021, 9(9), 1954; https://doi.org/10.3390/microorganisms9091954 - 14 Sep 2021
Viewed by 2378
Abstract
Myxococcus xanthus bacteria are a model system for understanding pattern formation and collective cell behaviors. When starving, cells aggregate into fruiting bodies to form metabolically inert spores. During predation, cells self-organize into traveling cell-density waves termed ripples. Both phase-contrast and fluorescence microscopy are [...] Read more.
Myxococcus xanthus bacteria are a model system for understanding pattern formation and collective cell behaviors. When starving, cells aggregate into fruiting bodies to form metabolically inert spores. During predation, cells self-organize into traveling cell-density waves termed ripples. Both phase-contrast and fluorescence microscopy are used to observe these patterns but each has its limitations. Phase-contrast images have higher contrast, but the resulting image intensities lose their correlation with cell density. The intensities of fluorescence microscopy images, on the other hand, are well-correlated with cell density, enabling better segmentation of aggregates and better visualization of streaming patterns in between aggregates; however, fluorescence microscopy requires the engineering of cells to express fluorescent proteins and can be phototoxic to cells. To combine the advantages of both imaging methodologies, we develop a generative adversarial network that converts phase-contrast into synthesized fluorescent images. By including an additional histogram-equalized output to the state-of-the-art pix2pixHD algorithm, our model generates accurate images of aggregates and streams, enabling the estimation of aggregate positions and sizes, but with small shifts of their boundaries. Further training on ripple patterns enables accurate estimation of the rippling wavelength. Our methods are thus applicable for many other phenotypic behaviors and pattern formation studies. Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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16 pages, 2434 KiB  
Communication
Assessment of Evolutionary Relationships for Prioritization of Myxobacteria for Natural Product Discovery
Microorganisms 2021, 9(7), 1376; https://doi.org/10.3390/microorganisms9071376 - 24 Jun 2021
Cited by 6 | Viewed by 3568
Abstract
Discoveries of novel myxobacteria have started to unveil the potentially vast phylogenetic diversity within the family Myxococcaceae and have brought about an updated approach to myxobacterial classification. While traditional approaches focused on morphology, 16S gene sequences, and biochemistry, modern methods including comparative genomics [...] Read more.
Discoveries of novel myxobacteria have started to unveil the potentially vast phylogenetic diversity within the family Myxococcaceae and have brought about an updated approach to myxobacterial classification. While traditional approaches focused on morphology, 16S gene sequences, and biochemistry, modern methods including comparative genomics have provided a more thorough assessment of myxobacterial taxonomy. Herein, we utilize long-read genome sequencing for two myxobacteria previously classified as Archangium primigenium and Chondrococcus macrosporus, as well as four environmental myxobacteria newly isolated for this study. Average nucleotide identity and digital DNA–DNA hybridization scores from comparative genomics suggest previously classified as A. primigenium to instead be a novel member of the genus Melittangium, C. macrosporus to be a potentially novel member of the genus Corallococcus with high similarity to Corallococcus exercitus, and the four isolated myxobacteria to include another novel Corallococcus species, a novel Pyxidicoccus species, a strain of Corallococcus exiguus, and a potentially novel Myxococcus species with high similarity to Myxococcus stipitatus. We assess the biosynthetic potential of each sequenced myxobacterium and suggest that genus-level conservation of biosynthetic pathways support our preliminary taxonomic assignment. Altogether, we suggest that long-read genome sequencing benefits the classification of myxobacteria and improves determination of biosynthetic potential for prioritization of natural product discovery. Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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18 pages, 1755 KiB  
Article
Behavioral Interactions between Bacterivorous Nematodes and Predatory Bacteria in a Synthetic Community
Microorganisms 2021, 9(7), 1362; https://doi.org/10.3390/microorganisms9071362 - 23 Jun 2021
Cited by 4 | Viewed by 3063
Abstract
Theory and empirical studies in metazoans predict that apex predators should shape the behavior and ecology of mesopredators and prey at lower trophic levels. Despite the ecological importance of microbial communities, few studies of predatory microbes examine such behavioral res-ponses and the multiplicity [...] Read more.
Theory and empirical studies in metazoans predict that apex predators should shape the behavior and ecology of mesopredators and prey at lower trophic levels. Despite the ecological importance of microbial communities, few studies of predatory microbes examine such behavioral res-ponses and the multiplicity of trophic interactions. Here, we sought to assemble a three-level microbial food chain and to test for behavioral interactions between the predatory nematode Caenorhabditis elegans and the predatory social bacterium Myxococcus xanthus when cultured together with two basal prey bacteria that both predators can eat—Escherichia coli and Flavobacterium johnsoniae. We found that >90% of C. elegans worms failed to interact with M. xanthus even when it was the only potential prey species available, whereas most worms were attracted to pure patches of E. coli and F. johnsoniae. In addition, M. xanthus altered nematode predatory behavior on basal prey, repelling C. elegans from two-species patches that would be attractive without M. xanthus, an effect similar to that of C. elegans pathogens. The nematode also influenced the behavior of the bacterial predator: M. xanthus increased its predatory swarming rate in response to C. elegans in a manner dependent both on basal-prey identity and on worm density. Our results suggest that M. xanthus is an unattractive prey for some soil nematodes and is actively avoided when other prey are available. Most broadly, we found that nematode and bacterial predators mutually influence one another’s predatory behavior, with likely consequences for coevolution within complex microbial food webs. Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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20 pages, 2109 KiB  
Article
A Genomic Survey of Signalling in the Myxococcaceae
Microorganisms 2020, 8(11), 1739; https://doi.org/10.3390/microorganisms8111739 - 06 Nov 2020
Cited by 8 | Viewed by 2714
Abstract
As prokaryotes diverge by evolution, essential ‘core’ genes required for conserved phenotypes are preferentially retained, while inessential ‘accessory’ genes are lost or diversify. We used the recently expanded number of myxobacterial genome sequences to investigate the conservation of their signalling proteins, focusing on [...] Read more.
As prokaryotes diverge by evolution, essential ‘core’ genes required for conserved phenotypes are preferentially retained, while inessential ‘accessory’ genes are lost or diversify. We used the recently expanded number of myxobacterial genome sequences to investigate the conservation of their signalling proteins, focusing on two sister genera (Myxococcus and Corallococcus), and on a species within each genus (Myxococcus xanthus and Corallococcus exiguus). Four new C. exiguus genome sequences are also described here. Despite accessory genes accounting for substantial proportions of each myxobacterial genome, signalling proteins were found to be enriched in the core genome, with two-component system genes almost exclusively so. We also investigated the conservation of signalling proteins in three myxobacterial behaviours. The linear carotenogenesis pathway was entirely conserved, with no gene gain/loss observed. However, the modular fruiting body formation network was found to be evolutionarily plastic, with dispensable components in all modules (including components required for fruiting in the model myxobacterium M. xanthus DK1622). Quorum signalling (QS) is thought to be absent from most myxobacteria, however, they generally appear to be able to produce CAI-I (cholerae autoinducer-1), to sense other QS molecules, and to disrupt the QS of other organisms, potentially important abilities during predation of other prokaryotes. Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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Review

Jump to: Editorial, Research

25 pages, 2944 KiB  
Review
Myxobacterial Genomics and Post-Genomics: A Review of Genome Biology, Genome Sequences and Related ‘Omics Studies
Microorganisms 2021, 9(10), 2143; https://doi.org/10.3390/microorganisms9102143 - 13 Oct 2021
Cited by 12 | Viewed by 2700
Abstract
Myxobacteria are fascinating and complex microbes. They prey upon other members of the soil microbiome by secreting antimicrobial proteins and metabolites, and will undergo multicellular development if starved. The genome sequence of the model myxobacterium Myxococcus xanthus DK1622 was published in 2006 and [...] Read more.
Myxobacteria are fascinating and complex microbes. They prey upon other members of the soil microbiome by secreting antimicrobial proteins and metabolites, and will undergo multicellular development if starved. The genome sequence of the model myxobacterium Myxococcus xanthus DK1622 was published in 2006 and 15 years later, 163 myxobacterial genome sequences have now been made public. This explosion in genomic data has enabled comparative genomics analyses to be performed across the taxon, providing important insights into myxobacterial gene conservation and evolution. The availability of myxobacterial genome sequences has allowed system-wide functional genomic investigations into entire classes of genes. It has also enabled post-genomic technologies to be applied to myxobacteria, including transcriptome analyses (microarrays and RNA-seq), proteome studies (gel-based and gel-free), investigations into protein–DNA interactions (ChIP-seq) and metabolism. Here, we review myxobacterial genome sequencing, and summarise the insights into myxobacterial biology that have emerged as a result. We also outline the application of functional genomics and post-genomic approaches in myxobacterial research, highlighting important findings to emerge from seminal studies. The review also provides a comprehensive guide to the genomic datasets available in mid-2021 for myxobacteria (including 24 genomes that we have sequenced and which are described here for the first time). Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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22 pages, 2608 KiB  
Review
Light-Triggered Carotenogenesis in Myxococcus xanthus: New Paradigms in Photosensory Signaling, Transduction and Gene Regulation
Microorganisms 2021, 9(5), 1067; https://doi.org/10.3390/microorganisms9051067 - 15 May 2021
Cited by 11 | Viewed by 3408
Abstract
Myxobacteria are Gram-negative δ-proteobacteria found predominantly in terrestrial habitats and often brightly colored due to the biosynthesis of carotenoids. Carotenoids are lipophilic isoprenoid pigments that protect cells from damage and death by quenching highly reactive and toxic oxidative species, like singlet oxygen, generated [...] Read more.
Myxobacteria are Gram-negative δ-proteobacteria found predominantly in terrestrial habitats and often brightly colored due to the biosynthesis of carotenoids. Carotenoids are lipophilic isoprenoid pigments that protect cells from damage and death by quenching highly reactive and toxic oxidative species, like singlet oxygen, generated upon growth under light. The model myxobacterium Myxococcus xanthus turns from yellow in the dark to red upon exposure to light because of the photoinduction of carotenoid biosynthesis. How light is sensed and transduced to bring about regulated carotenogenesis in order to combat photooxidative stress has been extensively investigated in M. xanthus using genetic, biochemical and high-resolution structural methods. These studies have unearthed new paradigms in bacterial light sensing, signal transduction and gene regulation, and have led to the discovery of prototypical members of widely distributed protein families with novel functions. Major advances have been made over the last decade in elucidating the molecular mechanisms underlying the light-dependent signaling and regulation of the transcriptional response leading to carotenogenesis in M. xanthus. This review aims to provide an up-to-date overview of these findings and their significance. Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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12 pages, 916 KiB  
Review
Myxococcus xanthus as a Model Organism for Peptidoglycan Assembly and Bacterial Morphogenesis
Microorganisms 2021, 9(5), 916; https://doi.org/10.3390/microorganisms9050916 - 24 Apr 2021
Cited by 3 | Viewed by 3125
Abstract
A fundamental question in biology is how cell shapes are genetically encoded and enzymatically generated. Prevalent shapes among walled bacteria include spheres and rods. These shapes are chiefly determined by the peptidoglycan (PG) cell wall. Bacterial division results in two daughter cells, whose [...] Read more.
A fundamental question in biology is how cell shapes are genetically encoded and enzymatically generated. Prevalent shapes among walled bacteria include spheres and rods. These shapes are chiefly determined by the peptidoglycan (PG) cell wall. Bacterial division results in two daughter cells, whose shapes are predetermined by the mother. This makes it difficult to explore the origin of cell shapes in healthy bacteria. In this review, we argue that the Gram-negative bacterium Myxococcus xanthus is an ideal model for understanding PG assembly and bacterial morphogenesis, because it forms rods and spheres at different life stages. Rod-shaped vegetative cells of M. xanthus can thoroughly degrade their PG and form spherical spores. As these spores germinate, cells rebuild their PG and reestablish rod shape without preexisting templates. Such a unique sphere-to-rod transition provides a rare opportunity to visualize de novo PG assembly and rod-like morphogenesis in a well-established model organism. Full article
(This article belongs to the Special Issue Myxobacteria: Physiology and Regulation)
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