Myxococcus xanthus

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Myxococcus xanthus
M. xanthus development.png
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Myxococcota
Class: Myxococcia
Order: Myxococcales
Family: Myxococcaceae
Genus: Myxococcus
Species:
M. xanthus
Binomial name
Myxococcus xanthus
Beebe 1941

Myxococcus xanthus is a gram-negative, bacillus (or rod-shaped) species of myxobacteria that is typically found in the top-most layer of soil. These bacteria lack flagella; rather, they use pili for motility. [1] M. xanthus is well-known for its predatory behavior on other microorganisms. These bacteria source carbon from lipids rather than sugars. They exhibit various forms of self-organizing behavior in response to environmental cues. Under normal conditions with abundant food, they exist as predatory, saprophytic single-species biofilm called a swarm, [2] highlighting the importance of intercellular communication for these bacteria. Under starvation conditions, they undergo a multicellular development cycle. [3]

Microbiology

Morphology

M. xanthus appear as gram-negative rods without flagella. [4] These rods have an average length of 7 microns and width of 0.5 microns. [5] It utilizes type IV pilus (T4P) to move in a "gliding" manner, crawling along a surface. [6] As a colony or swarm, M. xanthus appear as a thin layer of ripples, often moving toward prey. In its spore form, the bacterium becomes a sphere with a thick outer membrane. This spore is yellow-orange, giving M. xanthus its name (xanthós, Ancient Greek meaning "golden"). [4]

Environment

M. xanthus is typically found in the top most layer of soil, preying as a "pack" on other microorganisms like bacteria or fungi. [7] It is a neutralophile, growing best between a pH of 7.2-8.2. [8] The bacteria is characterized as a mesophile, growing best within the temperature range of 34-36°C. Like other Myxococcus bacteria, it is an obligate aerobe, meaning it requires oxygen for aerobic respiration to maintain cellular functions. [9]

Metabolism

M. xanthus is a chemoorganoheterotroph. It obtains energy from oxidation-reduction reactions and obtains both electrons and carbon from organic molecules. This bacteria does produce and consume glycogen, a branched glucose polymer, but cannot fully convert glucose to pyruvate though the Embden-Meyerhof-Parnas pathway. The flux through the pathway is incomplete, even though homologs of each enzyme are present in the genome. Because of this reason, M. xanthus cannot rely on sugars for growth. It is hypothesized that the incomplete glycolytic pathway produces substrates needed for lipid metabolism. [10]

M. xanthus relies on lipid metabolism to source carbon. The bacteria demonstrate a diverse set of lipid reactions, especially in lipid anabolism. It produces ether lipids, which are commonly associated with eukaryotes rather than prokaryotes. In these reactions, phospholipids are broken down into the polar head group, glycerol, and the two fatty acids. The fatty acids are degraded through β-oxidation at the carboxyl end of the fatty acid. M. xanthus expresses a wide variety of fatty acids. The calls contain at least 18 different fatty acids, compared to the 3 to 5 fatty acids seen in most Proteobacteria. Redundancy in the fatty acid elongation enzymes and desaturase enzymes may contribute to this diversity of fatty acids. [10]

M. xanthus salvages purines and pyrimidines from its prey to produce nucleic acids. Amino acids are treated similarly, with the majority undergoing further catalysis for use in other pathways as needed. [10]

Evolution

In 2003, two scientists, Velicer and Yu, deleted certain parts of the M. xanthus genome. This deletion made it unable to swarm effectively on soft agar. Individuals were cloned and allowed to evolve. After a period of 64 weeks, two of the evolving populations had started to swarm outward almost as effectively as normal wild-type colonies. However, the patterns of the swarm were very different from those of the wild-type bacteria. This suggested that they had developed a new way of moving, and Velicer and Yu confirmed this by showing that the new populations had not regained the ability to make pili, which allows wild-type bacteria to swarm. This study addressed questions about the evolution of cooperation between individuals that had plagued scientists for years. [11]

The evolution of M. xanthus can largely be attributed to two mechanisms of gene transfer such as LGT and vertical gene transfer. In this myxobacteria, LGT suggests acquisition of genes comes from other species of bacteria and this is also supported with the fact that the trait of M. xanthus' fruiting body is not possible without alien genes. [12] LGT has shown to be responsible for the expansion of the genome by at least 1.4 Mb. [13] Very little is known about the evolutionary mechanisms present in M. xanthus. However, it has been discovered that it can establish a generalist predator relationship with different prey, among which is Escherichia coli . In this predator-prey relationship, a parallel evolution of both species is observed through genomic and phenotypic modifications, producing in subsequent generations a better adaptation of one of the species that is counteracted by the evolution of the other, following a co-evolutionary model known as the Red Queen hypothesis. However, the evolutionary mechanisms present in M. xanthus that produce this parallel evolution are still unknown. [14]

Genetics

The genome of M. xanthus consists of one circular chromosome with one origin of replication and no plasmids. In 2001, the genome of strain DK1622 was determined to have 9.14 Mb. The genome size is considerably larger than other Proteobacteria, likely due to lineage-specific gene duplication. Over 90% of the genome contains genes that encode for proteins. [15]

In 2023, the R31 isolate of M. xanthus underwent whole genome sequencing amounting to 9.25Mb. The R31 isolate’s genome codes for roughly 55% core proteins, 25% accessory proteins, 13% specific proteins, and 10% proteins that are specific to the isolate. Strain-specific genes likely relate to the evolutionary and predatory aspects that are not found in other strains. Within the R31 genome, 18 distinct genomic islands and 11 prophages were found. Genomic islands were incorporated into the M. xanthus genome through horizontal gene transfer, thus altering the adaptability of the bacteria. Prophages, fragments of bacteriophage genetic material, can provide virulence factors that can increase antibiotic resistance and adaptability. [16]

Strains

  • Myxococcus xanthus DK1622
  • Myxococcus xanthus DZ2 v2
  • Myxococcus xanthus DZ2 v1
  • Myxococcus xanthus DZF1
  • Myxococcus xanthus NewJersey2
  • Myxococcus xanthus DSM16,526T
  • Myxococcus xanthus R31
  • Myxococcus xanthus KF4.3.9c1
  • Myxococcus xanthus ATCC 27,925
  • Myxococcus xanthus GH3.5.6c2
  • Myxococcus xanthus MC3.5.9c15
  • Myxococcus xanthus MC3.3.5c16
  • Myxococcus xanthus GH5.1.9c20
  • Myxococcus xanthus KF3.2.8c11
  • Myxococcus xanthus DK1622pDPO
  • Myxococcus xanthus AB023
  • Myxococcus xanthus AM005
  • Myxococcus xanthus CA029
  • Myxococcus xanthus AM003 [16]

Whole genome comparisons have indicated that M. virescens is the same species as M. xanthus. [17] M. virescens was first described in 1892, so has precedence. [18]

Complex Behaviors

Colony growth

A swarm of M. xanthus is a distributed system containing millions of bacteria that communicate among themselves in a non-centralized fashion. Simple patterns of cooperative behavior among the members of the colony combine to generate complex group behaviors in a process known as "stigmergy". For example, the tendency for one cell to glide only when in direct contact with another results in the colony forming swarms called "wolf-packs" that may measure up to several inches wide. This behavior is advantageous to the members of the swarm, as it increases the concentration of extracellular digestive enzymes secreted by the bacteria, thus facilitating predatory feeding. M. xanthus feeds on dead biomass of a broad range of bacteria and some fungi, discriminating living cells from dead cells and causing cell death and lysis when required. [19] [20]

During stressful conditions, the bacteria undergo a process in which about 100,000 individual cells aggregate to form a structure called the fruiting body over the course of approximately twenty-four hours. [21] The start of this process involves the cells displaying low motility. After several hours, the cells suddenly undergo a fast period of motion in which cells form "streams" to increase cell density and begin forming layers to develop the fruiting body. [21] On the interior of the fruiting body, the rod-shaped cells are differentiated into spherical, thick-walled spores. They undergo changes in the synthesis of new proteins, as well as alterations in the cell wall, which parallel the morphological changes. During these aggregations, dense ridges of cells move in ripples, which wax and wane over 5 hours. [22]

Motility

Social motility leads to a spatial distribution of cells with many clusters and few isolated single cells.

M. xanthus exhibits two main types of motility, known as A-motility and S-motility. A-motility (adventurous), otherwise known as "gliding," [23] is a method of locomotion that allows for forward movement on single cells, without the help of flagella, on a solid surface. [24] There are more than 37 genes involved in the A-motility system. This form of motility is facilitated by Glt complexes in the cell envelope of the cell, which is powered using a molecular motor called an Agl. The molecular motors in M. xanthus are driven by the H+ ion gradient. Each bacterial cell has an array of motors along the cell body, which are localized to the periplasmic space in the cell envelope but bound to the peptidoglycan layer in the cell wall. The motors are hypothesized to move on helical cytoskeletal filaments. [25]

The combination of the Glt complexes with the Agl motor allows for focal adhesion and move freely in the outer membrane, and provide contact with the substratum. Extracellular polysaccharide slime assists with the gliding movement across a surface. This bacteria is limited to forward movement and contains a lagging pole on the end, which opposes the motion. [26]

M. xanthus has the ability to use a second type of motility. This motility is called Social motility (S-motility), in which single cells do not move, but rather cells that are closer together move. This leads to a spatial distribution of cells with many clusters and few isolated single cells. [24] This motility depends on the presence of the Type IV pili [27] and diverse polysaccharides. [28] [29]

S-motility may represent a variation of twitching motility since it is mediated by the extension and retraction of type IV pili that extend through the leading cell pole. The genes of the S-motility system appear to be homologs of genes involved in the biosynthesis, assembly, and function of twitching motility in other bacteria. [30] [31]

Cell differentiation, fruiting and sporulation

In the presence of prey (here E. coli), M. xanthus cells self-organize into periodic bands of traveling waves, termed ripples (left-hand side). In the areas without prey, M. xanthus cells are under nutrient stress and as a result self-organize into haystack-shaped, spore-filled structures termed fruiting bodies (right-hand side, yellow mounds). Myxococcus xanthus rippling.png
In the presence of prey (here E. coli), M. xanthus cells self-organize into periodic bands of traveling waves, termed ripples (left-hand side). In the areas without prey, M. xanthus cells are under nutrient stress and as a result self-organize into haystack-shaped, spore-filled structures termed fruiting bodies (right-hand side, yellow mounds).

In response to starvation, since myxobacteria are neither chemolithotrophs nor autotrophs, they direct their resources to develop species-specific multicellular fruiting bodies that are capable of aiding in social cooperation for predation. [32] Starting from a uniform swarm of cells, some aggregate into fruiting bodies, while other cells remain in a vegetative state. Those cells that participate in the formation of the fruiting body transform from rods into spherical, heat-resistant myxospores, while the peripheral cells remain rod-shaped. [33] Although they are not as tolerant to environmental extremes as Bacillus endospores, the relative resistance of myxospores to desiccation and freezing enables myxobacteria to survive seasonally harsh environments. When a nutrient source becomes once again available, the myxospores germinate, shedding their spore coats to emerge into rod-shaped vegetative cells. The synchronized germination of thousands of myxospores from a single fruiting body enables the members of the new colony of myxobacteria to immediately engage in cooperative feeding. [34]

M. xanthus cells can also differentiate into environmentally-resistant spores in a starvation-independent manner. This process, known as chemically induced sporulation, is triggered by the presence of glycerol and other chemical compounds at high concentrations. [35] The biological implications of this sporulation process have been controversial for decades due to the unlikeliness of finding such high concentrations of chemical inducers in their natural environment. [36] [37] However, the finding that the antifungal compound ambruticin acts as a potent natural inducer at concentrations expected to be present in soil, suggests that chemically induced sporulation is the result of competition and communication with the ambruticin-producing myxobacterium Sorangium cellulosum. [38]

Sensing environmental signals

Ability to eavesdrop

It has been shown that an M. xanthus swarm is capable of eavesdropping on the extracellular signals that are produced by the bacteria it preys upon, leading to changes in swarm behavior and increasing its efficiency as a predator. In the presence of acyl homoserine lactones, which are the signals produced by prey intended for other prey, M. xanthus transforms toward more vegetative predatory cells instead of myxospores. This allows for highly adaptive physiology that will have likely contributed to the near ubiquitous distribution of the myxobacteria. These bacteria also respond to a chemoattractant called phosphatidylethanolamine, which is expelled when the prey dies. The chemoattractant draws in more M. xanthus, allowing for total lysis of prey cells. In order for M. xanthus to eavesdrop, there needs to be a high concentration of signals emitting between prey, which can occur when phosphatidylethanolamine is released, thus attracting more prey. [39]

Intercellular communication

It is very likely that cells communicate during the process of fruiting and sporulation because a starving group of cells forms myxospores within fruiting bodies. [40] Intercellular signaling appears to be necessary to ensure that sporulation happens in the proper place and at the proper time. [41] Research supports the existence of an extracellular signal, A-factor, which is necessary for developmental gene expression and for the development of a complete fruiting body. [42] This signaling mechanism is additionally capable of measuring the size of the surrounding aggregates. [21]

Developmental cheating

Social cheating exists among M. xanthus commonly. As long as mutants are not common and they are unable to perform the group beneficial function of producing spores, they will still reap the benefit of the population as a whole. Research has shown that four different types of M. xanthus mutants showed forms of cheating during development by being over-represented among spores relative to their initial frequency in the mixture. [43]

Importance in research

The complex life cycles of the myxobacteria make them very attractive models for the study of gene regulation as well as cell to cell interactions. The traits of M. xanthus make it very easy to study and, therefore, important to research. Laboratory strains of M. xanthus are available that are capable of planktonic growth in shaker culture, so they are easy to grow in large numbers. The tools of classical and molecular genetics are relatively well-developed in M. xanthus. [44]

Although the fruiting bodies of M. xanthus are relatively primitive compared with the elaborate structures produced by Stigmatella aurantiaca and other myxobacteria, the great majority of genes known to be involved in development are conserved across species. [45] In order to make agar cultures of M. xanthus grow into fruiting bodies, one simply can plate the bacteria on starvation media. [46] It is possible to artificially induce the production of myxospores without the intervening formation of fruiting bodies by adding compounds such as glycerol or various metabolites to the medium. [47] In this way, different stages in the developmental cycle can be experimentally isolated.

Related Research Articles

<span class="mw-page-title-main">Pilus</span> A proteinaceous hair-like appendage on the surface of bacteria

A pilus is a hair-like appendage found on the surface of many bacteria and archaea. The terms pilus and fimbria can be used interchangeably, although some researchers reserve the term pilus for the appendage required for bacterial conjugation. All conjugative pili are primarily composed of pilin – fibrous proteins, which are oligomeric.

<span class="mw-page-title-main">Myxobacteria</span> Order of bacteria

The myxobacteria are a group of bacteria that predominantly live in the soil and feed on insoluble organic substances. The myxobacteria have very large genomes relative to other bacteria, e.g. 9–10 million nucleotides except for Anaeromyxobacter and Vulgatibacter. One species of myxobacteria, Minicystis rosea, has the largest known bacterial genome with over 16 million nucleotides. The second largest is another myxobacteria Sorangium cellulosum.

<span class="mw-page-title-main">Multicopy single-stranded DNA</span>

Multicopy single-stranded DNA (msDNA) is a type of extrachromosomal satellite DNA that consists of a single-stranded DNA molecule covalently linked via a 2'-5'phosphodiester bond to an internal guanosine of an RNA molecule. The resultant DNA/RNA chimera possesses two stem-loops joined by a branch similar to the branches found in RNA splicing intermediates. The coding region for msDNA, called a "retron", also encodes a type of reverse transcriptase, which is essential for msDNA synthesis.

Sorangium cellulosum is a soil-dwelling Gram-negative bacterium of the group myxobacteria. It is motile and shows gliding motility. Under stressful conditions this motility, as in other myxobacteria, the cells congregate to form fruiting bodies and differentiate into myxospores. These congregating cells make isolation of pure culture and colony counts on agar medium difficult as the bacterium spread and colonies merge. It has an unusually-large genome of 13,033,779 base pairs, making it the largest bacterial genome sequenced to date by roughly 4 Mb.

<span class="mw-page-title-main">Bacteria</span> Domain of microorganisms

Bacteria are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were among the first life forms to appear on Earth, and are present in most of its habitats. Bacteria inhabit soil, water, acidic hot springs, radioactive waste, and the deep biosphere of Earth's crust. Bacteria play a vital role in many stages of the nutrient cycle by recycling nutrients and the fixation of nitrogen from the atmosphere. The nutrient cycle includes the decomposition of dead bodies; bacteria are responsible for the putrefaction stage in this process. In the biological communities surrounding hydrothermal vents and cold seeps, extremophile bacteria provide the nutrients needed to sustain life by converting dissolved compounds, such as hydrogen sulphide and methane, to energy. Bacteria also live in mutualistic, commensal and parasitic relationships with plants and animals. Most bacteria have not been characterised and there are many species that cannot be grown in the laboratory. The study of bacteria is known as bacteriology, a branch of microbiology.

<span class="mw-page-title-main">Swarming motility</span>

Swarming motility is a rapid and coordinated translocation of a bacterial population across solid or semi-solid surfaces, and is an example of bacterial multicellularity and swarm behaviour. Swarming motility was first reported by Jorgen Henrichsen and has been mostly studied in genus Serratia, Salmonella, Aeromonas, Bacillus, Yersinia, Pseudomonas, Proteus, Vibrio and Escherichia.

<span class="mw-page-title-main">Bacterial motility</span> Ability of bacteria to move independently using metabolic energy

Bacterial motility is the ability of bacteria to move independently using metabolic energy. Most motility mechanisms that evolved among bacteria also evolved in parallel among the archaea. Most rod-shaped bacteria can move using their own power, which allows colonization of new environments and discovery of new resources for survival. Bacterial movement depends not only on the characteristics of the medium, but also on the use of different appendages to propel. Swarming and swimming movements are both powered by rotating flagella. Whereas swarming is a multicellular 2D movement over a surface and requires the presence of surfactants, swimming is movement of individual cells in liquid environments.

<span class="mw-page-title-main">Gliding motility</span>

Gliding motility is a type of translocation used by microorganisms that is independent of propulsive structures such as flagella, pili, and fimbriae. Gliding allows microorganisms to travel along the surface of low aqueous films. The mechanisms of this motility are only partially known.

<span class="mw-page-title-main">Pxr sRNA</span>

Pxr sRNA is a regulatory RNA which downregulates genes responsible for the formation of fruiting bodies in Myxococcus xanthus. Fruiting bodies are aggregations of myxobacteria formed when nutrients are scarce, the fruiting bodies permit a small number of the aggregated colony to transform into stress-resistant spores.

Stigmatella aurantiaca is a member of myxobacteria, a group of gram-negative bacteria with a complex developmental life cycle.

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<i>Myxococcus</i> Genus of bacteria

Myxococcus is a genus of bacteria in the family Myxococcaceae. Myxococci are Gram-negative, spore-forming, chemoorganotrophic, obligate aerobes. They are elongated rods with rounded or tapered ends, and they are nonflagellated. The cells move by gliding and can predate other bacteria. The genus has been isolated from soil.

<span class="mw-page-title-main">Protein S (Myxococcus xanthus)</span>

Protein S is a protein found in Myxococcus xanthus. Its name derives from being the "S" band in an alphabetical ordering of proteins run from Myxococcus xanthus cell contents on a SDS-denaturing gel. Its study was initially prompted by the huge increase in Protein S production during sporulation of Myxococcus xanthus.

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<span class="mw-page-title-main">Twitching motility</span> Form of crawling bacterial motility

Twitching motility is a form of crawling bacterial motility used to move over surfaces. Twitching is mediated by the activity of hair-like filaments called type IV pili which extend from the cell's exterior, bind to surrounding solid substrates, and retract, pulling the cell forwards in a manner similar to the action of a grappling hook. The name twitching motility is derived from the characteristic jerky and irregular motions of individual cells when viewed under the microscope. It has been observed in many bacterial species, but is most well studied in Pseudomonas aeruginosa, Neisseria gonorrhoeae and Myxococcus xanthus. Active movement mediated by the twitching system has been shown to be an important component of the pathogenic mechanisms of several species.

<span class="mw-page-title-main">Social motility</span>

Social motility describes the motile movement of groups of cells that communicate with each other to coordinate movement based on external stimuli. There are multiple varieties of each kingdom that express social motility that provides a unique evolutionary advantages that other species do not possess. This has made them lethal killers such as African trypanosomiasis, or Myxobacteria. These evolutionary advantages have proven to increase survival rate among socially motile bacteria whether it be the ability to evade predators or communication within a swarm to form spores for long term hibernation in times of low nutrients or toxic environments.

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Myxococcus llanfair­pwll­gwyn­gyll­go­gery­chwyrn­drobwll­llan­tysilio­gogo­gochensis is a gram-negative, rod-shaped species of myxobacteria found in soil. It is a predator on other bacteria.

<span class="mw-page-title-main">Cyanobacterial morphology</span> Form and structure of a phylum

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<span class="mw-page-title-main">Adventurous motility</span>

Adventurous motility is as a type of gliding motility; unlike most motility mechanisms, adventurous motility does not involve a flagellum. Gliding motility usually involves swarms of bacteria; however, adventurous motility is practiced by individual cells. This gliding is hypothesized to occur via assembly of a type IV secretion system and the extrusion of a polysaccharide slime, or by use of a series of adhesion complexes. The majority of research on adventurous motility has focused on the species, Myxococcus xanthus. The earliest of this research is attributed to Jonathan Hodgkin and Dale Kaiser.

References

  1. ↑ Dye, Keane J.; Salar, Safoura; Allen, Uvina; Smith, Wraylyn; Yang, Zhaomin (2023-09-26). Galperin, Michael Y. (ed.). "Myxococcus xanthus PilB interacts with c-di-GMP and modulates motility and biofilm formation". Journal of Bacteriology. 205 (9): e0022123. doi:10.1128/jb.00221-23. ISSN   0021-9193. PMC   10521364 . PMID   37695853.
  2. ↑ Thiery, Susanne; Kaimer, Christine (2020-01-14). "The Predation Strategy of Myxococcus xanthus". Frontiers in Microbiology. 11: 2. doi: 10.3389/fmicb.2020.00002 . ISSN   1664-302X. PMC   6971385 . PMID   32010119.
  3. ↑ Kroos, Lee; Kuspa, Adam; Kaiser, Dale (1986-09-01). "A global analysis of developmentally regulated genes in Myxococcus xanthus". Developmental Biology. 117 (1): 252–266. doi:10.1016/0012-1606(86)90368-4. ISSN   0012-1606. PMID   3017794.
  4. 1 2 Beebe, J. M. (August 1941). "The Morphology and Cytology of Myxococcus xanthus , N. Sp". Journal of Bacteriology. 42 (2): 193–223. doi:10.1128/jb.42.2.193-223.1941. ISSN   0021-9193. PMC   374753 . PMID   16560449.
  5. ↑ Kaiser, Dale; Robinson, Mark; Kroos, Lee (August 2010). "Myxobacteria, Polarity, and Multicellular Morphogenesis". Cold Spring Harbor Perspectives in Biology. 2 (8): a000380. doi:10.1101/cshperspect.a000380. ISSN   1943-0264. PMC   2908774 . PMID   20610548.
  6. ↑ Dye, Keane J.; Salar, Safoura; Allen, Uvina; Smith, Wraylyn; Yang, Zhaomin (2023-09-26). Galperin, Michael Y. (ed.). "Myxococcus xanthus PilB interacts with c-di-GMP and modulates motility and biofilm formation". Journal of Bacteriology. 205 (9): e0022123. doi:10.1128/jb.00221-23. ISSN   0021-9193. PMC   10521364 . PMID   37695853.
  7. ↑ Konovalova, Anna; Petters, Tobias; Søgaard-Andersen, Lotte (March 2010). "Extracellular biology of Myxococcus xanthus". FEMS Microbiology Reviews. 34 (2): 89–106. doi:10.1111/j.1574-6976.2009.00194.x. ISSN   1574-6976. PMID   19895646.
  8. ↑ Dworkin, Martin (August 1962). "Nutritional Requirements for Vegetative Growth of Myxococcus xanthus". Journal of Bacteriology. 84 (2): 250–257. doi:10.1128/jb.84.2.250-257.1962. ISSN   0021-9193. PMC   277848 . PMID   13888810.
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  10. 1 2 3 Curtis, Patrick D.; Shimkets, Lawrence J. (2014-04-09), Whitworth, David E. (ed.), "Metabolic Pathways Relevant to Predation, Signaling, and Development", Myxobacteria, Washington, DC, USA: ASM Press, pp. 241–258, doi:10.1128/9781555815677.ch14, ISBN   978-1-68367-155-8 , retrieved 2024-02-29
  11. ↑ Velicer, Gregory J.; Yu, Yuen-tsu N. (September 2003). "Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus". Nature. 425 (6953): 75–78. Bibcode:2003Natur.425...75V. doi:10.1038/nature01908. ISSN   1476-4687. PMID   12955143.
  12. ↑ Goldman, Barry; Bhat, Swapna; Shimkets, Lawrence J. (2007-12-26). Petrosino, Joseph (ed.). "Genome Evolution and the Emergence of Fruiting Body Development in Myxococcus xanthus". PLOS ONE. 2 (12): e1329. Bibcode:2007PLoSO...2.1329G. doi: 10.1371/journal.pone.0001329 . ISSN   1932-6203. PMC   2129111 . PMID   18159227.
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  14. ↑ Nair, Ramith R.; Vasse, Marie; Wielgoss, Sébastien; Sun, Lei; Yu, Yuen-Tsu N.; Velicer, Gregory J. (2019-09-20). "Bacterial predator-prey coevolution accelerates genome evolution and selects on virulence-associated prey defences". Nature Communications. 10 (1): 4301. Bibcode:2019NatCo..10.4301N. doi:10.1038/s41467-019-12140-6. ISSN   2041-1723. PMC   6754418 . PMID   31541093.
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