FIG 1
Phylogeny within the order Myxococcales and fruiting body morphologies. Dendrogram of members of the order Myxococcales. Species included in this study are indicated by the asterisks (*). A consensus sequence generated from an alignment of several nonMyxococcales 16S rRNA genes was used as the root of the tree. Bootstrap values (percentages) shown at nodes are based on 1,000 replications. The vertical bar to the right indicates the three suborders within the Myxococcales: light gray, Cystobacterineae; dark gray, Nannocystineae; and black, Sorangineae.
Source publication
Genetic programs underlying multicellular morphogenesis and cellular differentiation are most often associated with eukaryotic organisms, but examples also exist in bacteria such as the formation of multicellular, spore-filled fruiting bodies in the order Myxococcales. Most members of the Myxococcales undergo a multicellular developmental program c...
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Context 1
... Huntley et al. · doi:10.1093/molbev/msq292 resulting alignment was used to generate a bootstrapped (1,000 iterations) neighbor joining tree file from which the image shown in Figure 1 was generated using the Treedyn software ( Chevenet et al. 2006). The above analyses were repeated using the 16S rRNA sequences from all Deltapro- teobacteria with a completed genome sequence to pro- duce the tree figure shown in supplementary table S1 (Supplementary Material online). ...
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... 2CP-C ( Thomas et al. 2008) and 2CP-1, and Anaeromyxobacter species 109-5 and K. To decide which Anaerobacter genome to use in our analyses, we compared the four Anaerobacter genomes. The genomes of Anaeromyxobacter 2CP-C, 2CP-1, Fw109-5, and K con- tain 4,346, 4,473, 4,466, and 4,457 protein-coding sequen- ces, respectively (supplementary fig. S1, Supplementary Material online). Possible orthologs for each Anaeromyxo- bacter gene were identified using a reciprocal best BlastP hit method (see below). About 3,041 genes are conserved in all four genomes and represent 70%, 68%, 68%, and 68% of the genes in 2CP-C, 2CP-1, Fw109-5, and K, respectively (supplementary fig. S1, ...
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... (supplementary fig. S1, Supplementary Material online). Possible orthologs for each Anaeromyxo- bacter gene were identified using a reciprocal best BlastP hit method (see below). About 3,041 genes are conserved in all four genomes and represent 70%, 68%, 68%, and 68% of the genes in 2CP-C, 2CP-1, Fw109-5, and K, respectively (supplementary fig. S1, Supplementary Material online). About 7%, 6%, 26%, and 5% of all genes in the genomes of 2CP-C, 2CP-1, Fw109-5, and K, respectively, have no or- thologs in any of the other Anaeromyxobacter genomes. Be- cause the 2CP-C genome is the best-characterized of these four genomes ( Thomas et al. 2008) and appear to represent well all four ...
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... five species cover all three Myxococcales subor- ders: M. xanthus, S. aurantiaca, and A. dehalogenans belong to the Cystobacterineae, S. cellulosum belong to the Soran- gineae, and H. ochraceum belong to the Nannocystineae ( Fig. 1 and table 1) ( Shimkets et al. 2006). In all three sub- orders, species have been isolated, which initiate a develop- mental program resulting in fruiting body formation ( Shimkets et al. ...
Citations
... 9,10 Although distinct sporulation genes have been identified in other bacteria, such as Bacillus and Streptomyces, a conserved genetic blueprint for spore formation has not yet been discovered in myxobacteria. [11][12][13] Myxobacterial genome sequences revealed particularly large genomes that are especially rich in numbers of BGCs and encode structurally diverse and pharmacologically active specialized metabolites. 4,14 Although characterized metabolites range from large macrolides-such as epothilone (which inspired many analogs in development and clinical trials as anticancer drugs) and the antibiotic sorangicin over atypical peptides (as exemplified by the topoisomerase inhibitor cystobactamide)-to small terpenoids represented by the antiviral sandacrabins, the vast majority of the myxobacterial-specialized metabolome remains untapped. ...
... Within the active layer, seasonally incr eased pr okaryotic biomass could support higher predator abundances. We hypothesise that the spore-containing fruiting bodies in Myxococcota (Huntley et al. 2011 ) might resist the winter freeze-off, while the freeze-induced mortality of prey taxa might suppl y the gr owth substr ate for Myxococcota in spring (Bang-Andreasen et al. 2020 ). Bdellovibrionota abundances w ere lo w. ...
Permafrost soils store a substantial part of the global soil carbon and nitrogen. However, global warming causes abrupt erosion and gradual thaw, which make these stocks vulnerable to microbial decomposition into greenhouse gases. Here, we investigated the microbial response to abrupt in situ permafrost thaw. We sequenced the total RNA of a 1 m deep soil core consisting of up to 26 500-year-old permafrost material from an active abrupt erosion site. We analysed the microbial community in the active layer soil, the recently thawed, and the intact permafrost, and found maximum RNA:DNA ratios in recently thawed permafrost indicating a high microbial activity. In thawed permafrost, potentially copiotrophic Burkholderiales and Sphingobacteriales, but also microbiome predators dominated the community. Overall, both thaw-dependent and long-term soil properties significantly correlated with changes in community composition, as did microbiome predator abundance. Bacterial predators were dominated in shallower depths by Myxococcota, while protozoa, especially Cercozoa and Ciliophora, almost tripled in relative abundance in thawed layers. Our findings highlight the ecological importance of a diverse interkingdom and active microbial community highly abundant in abruptly thawing permafrost, as well as predation as potential biological control mechanism.
... This study explored 61 myxobacterial genomes, distributed within three suborders and nine families (58)(59)(60)(61)(62)(63)(64)(65)(66)(67)(68)(69)(70)(71), in addition to 59 outgroup genomes [members from 32 non-Myxococcales Deltaproteobacteria, 4 α-, 6 β-, 9 γ-, 4 £-proteobacteria, 2 Firmicutes, 1 Actinobacteria, and 1 FCB (Fibrobacteres, Chlorobi, and Bacteroidetes) group organism]. Highly conserved gapless concatenated alignment of 26 housekeeping protein sequences (68,72) was subjected to RAxML to build a maximum likelihood phylogenetic tree using JTT Substitution Matrix and 100 bootstrap values (73). ...
The predatory deltaproteobacterium Myxococcus xanthus uses a helically-trafficked motor at bacterial focal-adhesion (bFA) sites to power gliding motility. Using total internal reflection fluorescence and force microscopies, we identify the von Willebrand A domain-containing outer-membrane (OM) lipoprotein CglB as an essential substratum-coupling adhesin of the gliding transducer (Glt) machinery at bFAs. Biochemical and genetic analyses reveal that CglB localizes to the cell surface independently of the Glt apparatus; once there, it is recruited by the OM module of the gliding machinery, a heteroligomeric complex containing the integral OM β barrels GltA, GltB, and GltH, as well as the OM protein GltC and OM lipoprotein GltK. This Glt OM platform mediates the cell-surface accessibility and retention of CglB by the Glt apparatus. Together, these data suggest that the gliding complex promotes regulated surface exposure of CglB at bFAs, thus explaining the manner by which contractile forces exerted by inner-membrane motors are transduced across the cell envelope to the substratum.
... This phenomenon has been documented in a wide range of systems [71][72][73]. In the myxobacteria, the gene sets necessary for fruiting body development have diverged extensively across species [74,75]. At much shorter evolutionary timescales, analyses of an experimental lineage [76] and the natural variation at a regulatory region [50] have shown that the genetic pathways underlying M. xanthus development are evolutionarily malleable [77]. ...
Background:
Social defectors may meet diverse cooperators. Genotype-by-genotype interactions may constrain the ranges of cooperators upon which particular defectors can cheat, limiting cheater spread. Upon starvation, the soil bacterium Myxococcus xanthus cooperatively develops into spore-bearing fruiting bodies, using a complex regulatory network and several intercellular signals. Some strains (cheaters) are unable to sporulate effectively in pure culture due to mutations that reduce signal production but can exploit and outcompete cooperators within mixed groups.
Results:
In this study, interactions between a cheater disrupted at the signaling gene csgA and allopatrically diversified cooperators reveal a very small cheating range. Expectedly, the cheater failed to cheat on all natural-isolate cooperators owing to non-cheater-specific antagonisms. Surprisingly, some lab-evolved cooperators had already exited the csgA mutant's cheating range after accumulating fewer than 20 mutations and without experiencing cheating during evolution. Cooperators might also diversify in the potential for a mutation to reduce expression of a cooperative trait or generate a cheating phenotype. A new csgA mutation constructed in several highly diverged cooperators generated diverse sporulation phenotypes, ranging from a complete defect to no defect, indicating that genetic backgrounds can limit the set of genomes in which a mutation creates a defector.
Conclusions:
Our results demonstrate that natural populations may feature geographic mosaics of cooperators that have diversified in their susceptibility to particular cheaters, limiting defectors' cheating ranges and preventing them from spreading. This diversification may also lead to variation in the phenotypes generated by any given cooperation-gene mutation, further decreasing the chance of a cheater emerging which threatens the persistence of cooperation in the system.
... alkB and nah) . The MAG WB_200 was assigned to the order Myxococcales (Myxococcale_WB_200, Proteobacteria), that encompasses microorganisms capable of forming a fruiting body, a sporulation type with a relevant role during starvation and critical to face harsh environmental conditions (Huntley et al., 2011). The order Myxococcales comprises saprophytic microorganisms, typically found in surface environments and involved in the decomposition of polymers in biofilms (Shimkets et al., 2006). ...
Antarctica is the coldest and driest continent on Earth, characterized by polyextreme environmental conditions, where species adapted form complex networks of interactions. Microbial communities growing in these harsh environments can form biofilms that help the associated species to survive and thrive. A rich body of knowledge describes environmental biofilm communities; however, most studies have focused on dominant community members rather than functional complexity and metabolic potential. To overcome these limitations, the present study used genome-centric metagenomics to describe two biofilm samples subjected to different temperature collected in Deception Island, Maritime Antarctica. The results unraveled a complex biofilm microbiome represented by 180 metagenome-assembled genomes. The potential metabolic interactions were investigated using metabolic flux balance analysis and revealed that purple bacteria are the community members with the highest correlations with other bacteria. Due to their predicted mixotrophic behavior, they may play a crucial role in the microbiome, likely supporting the heterotrophic species in biofilms. Metatranscriptomics results revealed that the chaperone system and proteins counteracting ROS and toxic compounds have a major role in maintaining bacterial cell homeostasis in sediments of volcanic origin.
... In Proteobacteria, the formation of resistant specialized structures is known in the Azotobacter genus (Høidal et al., 2000;Rejman and Kozubek, 2004) and in the Myxococcales order (Kottel et al., 1975;Julien et al., 2000;Garcia et al., 2009;Huntley et al., 2011;Mohr et al., 2012). A member of the latter, the genus Sorangium, was enriched in the spore fraction of the microbial mats, while a second one (Phaselicystis) was enriched in the lake sediment samples. ...
The production of specialized resting cells is a remarkable strategy developed by several organisms to survive unfavorable environmental conditions. Spores are specialized resting cells that are characterized by low to absent metabolic activity and higher resistance. Spore-like cells are known from multiple groups of bacteria, which can form spores under suboptimal growth conditions (e.g., starvation). In contrast, little is known about the production of specialized resting cells in archaea. In this study, we applied a culture-independent method that uses physical and chemical lysis, to assess the diversity of lysis-resistant bacteria and archaea and compare it to the overall prokaryotic diversity (direct DNA extraction). The diversity of lysis-resistant cells was studied in the polyextreme environment of the Salar de Huasco. The Salar de Huasco is a high-altitude athalassohaline wetland in the Chilean Altiplano. Previous studies have shown a high diversity of bacteria and archaea in the Salar de Huasco, but the diversity of lysis-resistant microorganisms has never been investigated. The underlying hypothesis was that the combination of extreme abiotic conditions might favor the production of specialized resting cells. Samples were collected from sediment cores along a saline gradient and microbial mats were collected in small surrounding ponds. A significantly different diversity and composition were found in the sediment cores or microbial mats. Furthermore, our results show a high diversity of lysis-resistant cells not only in bacteria but also in archaea. The bacterial lysis-resistant fraction was distinct in comparison to the overall community. Also, the ability to survive the lysis-resistant treatment was restricted to a few groups, including known spore-forming phyla such as Firmicutes and Actinobacteria. In contrast to bacteria, lysis resistance was widely spread in archaea, hinting at a generalized resistance to lysis, which is at least comparable to the resistance of dormant cells in bacteria. The enrichment of Natrinema and Halarchaeum in the lysis-resistant fraction could hint at the production of cyst-like cells or other resistant cells. These results can guide future studies aiming to isolate and broaden the characterization of lysis-resistant archaea.
... These myxobacteria are soil-dwelling, except for the aquatic Enhygromyxa salina, Haliangium ochraceum and Plesiocystis pacifica, and obligate aerobes except for A. dehalogenans, a facultative anaerobe. Their GC-rich (66%-75%) genomes are among the largest in bacteria (~9-16 Mb) but are reduced, presumably by extensive gene loss, in V. incomptus (~4.4 Mb) and A. dehalogenans (~5 Mb) (Huntley et al., 2011;Yamamoto et al., 2014). BLAST searches of these genomes using CarA Mx or CarH Mx (35% identical) as query yielded one hit in Sorangiineae and Nannocystineae, and two hits in Cystobacterineae except for a single hit in Cystobacter ferrugineus, Cystobacter fuscus and Melittangium boletus, and none in A. dehalogenans or V. incomptus. ...
Light-induced carotenogenesis in Myxococcus xanthus is controlled by the B12 -based CarH repressor and photoreceptor, and by a separate intricate pathway involving singlet oxygen, the B12 -independent CarH paralog CarA and various other proteins, some eukaryotic-like. Whether other myxobacteria conserve these pathways and undergo photoregulated carotenogenesis is unknown. Here, comparative analyses across 27 Myxococcales genomes identified carotenogenic genes, albeit arranged differently, with carH often in their genomic vicinity, in all three Myxococcales suborders. However, CarA and its associated factors were found exclusively in suborder Cystobacterineae, with carA-carH invariably in tandem in a syntenic carotenogenic operon, except for Cystobacter/Melittangium, which lack CarA but retain all other factors. We experimentally show B12 -mediated photoregulated carotenogenesis in representative myxobacteria, and a remarkably plastic CarH operator design and DNA binding across Myxococcales. Unlike the two characterized CarH from other phyla, which are tetrameric, Cystobacter CarH (the first myxobacterial homolog amenable to analysis in vitro) is a dimer that combines direct CarH-like B12 -based photoregulation with CarA-like DNA-binding and inhibition by an antirepressor. This study provides new molecular insights into B12 -dependent photoreceptors. It further establishes the B12 -dependent pathway for photoregulated carotenogenesis as broadly prevalent across myxobacteria and its evolution, exclusively in one suborder, into a parallel complex B12 -independent circuit. This article is protected by copyright. All rights reserved.
... Like zygotic developmental systems, aggregative systems have complex genetic architectures and involve temporal cascades of cell-cell signalling resulting in cell-type differentiation. In the myxobacteria, fruiting body morphologies and their genetic foundations have diversified greatly [18,19] (figure 1a). Such morphological diversification may have been driven in part by variation in selective forces, whether abiotic, e.g. the physico-chemical character of soil surfaces [20], or biotic, e.g. the composition of prey communities [21] or social groups [22,23]. ...
... Our finding that distinct developmental partners can greatly impact morphological evolution in M. xanthus may help to understand the remarkable diversification of fruiting body morphologies observed across myxobacterial species (figure 1a). Distinct cellular compositions of spatially clustered lineage sets during natural cycles of development may have contributed significantly to this diversification by differentially impacting evolutionary trajectories [18,19]. Across a broader range of multicellular developmental systems, the cellular character of development may shape not only both deterministic and stochastic forms of morphological evolution, but also the evolution of phenotypic plasticity [48][49][50], developmental bias [51] and both the genetic basis [52] and evolvability of development [53,54]. ...
Aggregative multicellular development is a social process involving complex forms of cooperation among unicellular organisms. In some aggregative systems, development culminates in the construction of spore-packed fruiting bodies and often unfolds within genetically and behaviourally diverse conspecific cellular environments. Here, we use the bacterium Myxococcus xanthus to test whether the character of the cellular environment during aggregative development shapes its morphological evolution. We manipulated the cellular composition of Myxococcus development in an experiment in which evolving populations initiated from a single ancestor repeatedly co-developed with one of several non-evolving partners—a cooperator, three cheaters and three antagonists. Fruiting body morphology was found to diversify not only as a function of partner genotype but more broadly as a function of partner social character, with antagonistic partners selecting for greater fruiting body formation than cheaters or the cooperator. Yet even small degrees of genetic divergence between distinct cheater partners sufficed to drive treatment-level morphological divergence. Co-developmental partners also determined the magnitude and dynamics of stochastic morphological diversification and subsequent convergence. In summary, we find that even just a few genetic differences affecting developmental and social features can greatly impact morphological evolution of multicellular bodies and experimentally demonstrate that microbial warfare can promote cooperation.
... FruA activation depends on the MrpC-dependent fruA transcription in response to starvation and the intercellular C-signal; subsequently MrpC and FruA act coordinately and are essential for the downstream gene regulatory changes responsible for fruiting body formation [25,[28][29][30][31]. Ultimately these intra-and intercellular signals and transcription factors lead to the execution of this complex genetic program. Using genetics and global transcriptional profiling, hundreds of genes have been demonstrated to be developmentally regulated at the transcriptional level, many of which are important for development [23,[32][33][34][35][36][37][38][39][40][41]. ...
... Fruiting body morphology varies between species including haystack shaped as in M. xanthus, single sporangioles on a stalk like Myxococcus stipitatus, and complex stalked fruiting bodies topped with multiple sporangioles in Stigmatella aurantiaca and Corallococcus coralloides [42]. Previous work based on gene content comparisons has found that several essential developmental genes in M. xanthus are missing from the genomes of other fruiting Myxobacteria and with an inverse correlation between number of genes conserved and phylogenetic distance, suggesting that the genetic programs for fruiting body formation vary between Myxobacteria [32]. Moreover, experimental evolution experiments with M. xanthus have also showed that development can be restored to a fruitingdeficient mutant using a different transcriptional program than that in WT M. xanthus [43]. ...
... As a quality control of the RNAseq data, we observed that the expression patterns of four developmentally regulated genes matched those from previous reports, with spiA, fruA, and devT showing substantial early upregulation, and fmgE demonstrating transcription later during development ( Fig. 2a-d) [26,34,35,54]. We also looked more generally at expression in 95 previously identified genes specifically important for fruiting body formation and sporulation [32]. While some show dramatic increases in expression during development, many other genes show modest or less predictable expression patterns (Additional file 1). ...
Background
The Myxococcales are well known for their predatory and developmental social processes, and for the molecular complexity of regulation of these processes. Many species within this order have unusually large genomes compared to other bacteria, and their genomes have many genes that are unique to one specific sequenced species or strain. Here, we describe RNAseq based transcriptome analysis of the FruA regulon of Myxococcus xanthus and a comparative RNAseq analysis of two Myxococcus species, M. xanthus and Myxococcus stipitatus , as they respond to starvation and begin forming fruiting bodies.
Results
We show that both species have large numbers of genes that are developmentally regulated, with over half the genome showing statistically significant changes in expression during development in each species. We also included a non-fruiting mutant of M. xanthus that is missing the transcriptional regulator FruA to identify the direct and indirect FruA regulon and to identify transcriptional changes that are specific to fruiting and not just the starvation response. We then identified Interpro gene ontologies and COG annotations that are significantly up- or down-regulated during development in each species. Our analyses support previous data for M. xanthus showing developmental upregulation of signal transduction genes, and downregulation of genes related to cell-cycle, translation, metabolism, and in some cases, DNA replication. Gene expression in M. stipitatus follows similar trends. Although not all specific genes show similar regulation patterns in both species, many critical developmental genes in M. xanthus have conserved expression patterns in M. stipitatus , and some groups of otherwise unstudied orthologous genes share expression patterns.
Conclusions
By identifying the FruA regulon and identifying genes that are similarly and uniquely regulated in two different species, this work provides a more complete picture of transcription during Myxococcus development . We also provide an R script to allow other scientists to mine our data for genes whose expression patterns match a user-selected gene of interest.
... All three are typical myxobacterial genome sequences, being large (9-10.3 Mbp), with a high %GC content (>67%), sharing synteny with each other and with M. xanthus DK1622 [24][25][26]. M. fulvus HW-1 (reclassified as Myxococcus macrosporus HW-1 in October 2018) is a halotolerant marine strain which forms fruiting bodies in low salinity conditions, but which can sporulate without fruiting in saltwater [26]. C. coralloides DSM 2259 produces fruiting bodies resembling coral, and it belongs to the most common myxobacterial genus isolated from soils alongside Myxococcus [27]. ...
... C. coralloides DSM 2259 produces fruiting bodies resembling coral, and it belongs to the most common myxobacterial genus isolated from soils alongside Myxococcus [27]. S. aurantiaca DW4/3-1 was first sequenced in draft form (released as 579 contigs in Sep 2006), before having its genome completely sequenced four years later [24]. Like C. coralloides DSM 2259, S. aurantiaca DW4/3-1 also produces morphologically complex fruiting bodies-in this case, with sporangioles mounted on a stalk. ...
... Like C. coralloides DSM 2259, S. aurantiaca DW4/3-1 also produces morphologically complex fruiting bodies-in this case, with sporangioles mounted on a stalk. Comparisons with the genome sequences of other fruiting myxobacteria showed a lack of conservation of genes involved in fruiting across these myxobacteria, implying the genetic program underlying multicellular development is much more plastic than had been expected [24]. ...
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).
