Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies

Claessen, Dennis; Rozen, Daniel E.; Kuipers, Oscar P.; Søgaard‐Andersen, Lotte; Wezel, Gilles P. van

doi:10.1038/nrmicro3178

Cited by 404 publications

(426 citation statements)

References 113 publications

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“…Exponential growth of the vegetative hyphae is achieved by a combination of tip growth and branching. The fact that cell division during vegetative growth does not lead to cell fission but rather to cross-walls that separate the hyphae into connected compartments (176) makes streptomycetes a rare example of a multicellular bacterium, with each compartment containing multiple copies of the chromosome (177,178). The spacing of the vegetative cross-walls varies significantly, both between different Streptomyces species and within individual species between different growth conditions and mycelial ages.…”

Section: The Streptomyces Life Cyclementioning

confidence: 99%

Taxonomy, Physiology, and Natural Products of Actinobacteria

Barka

Vatsa

Sanchez

et al. 2016

Microbiol Mol Biol Rev

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1,530

1,048

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SUMMARYActinobacteriaare Gram-positive bacteria with high G+C DNA content that constitute one of the largest bacterial phyla, and they are ubiquitously distributed in both aquatic and terrestrial ecosystems. ManyActinobacteriahave a mycelial lifestyle and undergo complex morphological differentiation. They also have an extensive secondary metabolism and produce about two-thirds of all naturally derived antibiotics in current clinical use, as well as many anticancer, anthelmintic, and antifungal compounds. Consequently, these bacteria are of major importance for biotechnology, medicine, and agriculture.Actinobacteriaplay diverse roles in their associations with various higher organisms, since their members have adopted different lifestyles, and the phylum includes pathogens (notably, species ofCorynebacterium,Mycobacterium,Nocardia,Propionibacterium, andTropheryma), soil inhabitants (e.g.,MicromonosporaandStreptomycesspecies), plant commensals (e.g.,Frankiaspp.), and gastrointestinal commensals (Bifidobacteriumspp.).Actinobacteriaalso play an important role as symbionts and as pathogens in plant-associated microbial communities. This review presents an update on the biology of this important bacterial phylum.

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Section: The Streptomyces Life Cyclementioning

confidence: 99%

Taxonomy, Physiology, and Natural Products of Actinobacteria

Barka

Vatsa

Sanchez

et al. 2016

Microbiol Mol Biol Rev

Self Cite

1,530

1,048

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“…Robust control of CsgD production is clearly important, given that Ͼ30% of the genes in the genome were differentially expressed between the S. Typhimurium multicellular aggregates and planktonic cells. The large number of differentially expressed genes represents a tremendous amount of nonheritable genetic change, on the order of a developmental program in bacteria (74). Since only 20 CsgD-specific targets were identified in a recent E. coli chromatin immunoprecipitation sequencing (ChIP-seq) study (75), we hypothesize that CsgD initiates the aggregation process and that a cascade of gene expression changes follows as cells produce an extracellular matrix (35).…”

Section: Discussionmentioning

confidence: 99%

Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence

MacKenzie

Wang²,

Shivak

et al. 2015

Infect Immun

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f Pathogenic bacteria often need to survive in the host and the environment, and it is not well understood how cells transition between these equally challenging situations. For the human and animal pathogen Salmonella enterica serovar Typhimurium, biofilm formation is correlated with persistence outside a host, but the connection to virulence is unknown. In this study, we analyzed multicellular-aggregate and planktonic-cell subpopulations that coexist when S. Typhimurium is grown under biofilminducing conditions. These cell types arise due to bistable expression of CsgD, the central biofilm regulator. Despite being exposed to the same stresses, the two cell subpopulations had 1,856 genes that were differentially expressed, as determined by transcriptome sequencing (RNA-seq). Aggregated cells displayed the characteristic gene expression of biofilms, whereas planktonic cells had enhanced expression of numerous virulence genes. Increased type three secretion synthesis in planktonic cells correlated with enhanced invasion of a human intestinal cell line and significantly increased virulence in mice compared to the aggregates. However, when the same groups of cells were exposed to desiccation, the aggregates survived better, and the competitive advantage of planktonic cells was lost. We hypothesize that CsgD-based differentiation is a form of bet hedging, with single cells primed for host cell invasion and aggregated cells adapted for persistence in the environment. This allows S. Typhimurium to spread the risks of transmission and ensures a smooth transition between the host and the environment.

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“…The eusocial insects can be divided depending upon whether the evolution of eusociality was driven by either the advantage in forming defensive groups (e.g., termites, aphids) or the efficiency benefit gained from cooperating to rear young (e.g., hymenoptera) (17). The ecological benefits to multicellularity seem to divide along analogous lines due to the benefits of forming defensive groups (e.g., algae) or to make certain traits more efficient (e.g., yeast, slime molds) (13,64). Can we make similar generalizations about the transitions between species?…”

Section: Pragmatismmentioning

confidence: 99%

Major evolutionary transitions in individuality

West

Fisher

Gardner

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

314

412

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The evolution of life on earth has been driven by a small number of major evolutionary transitions. These transitions have been characterized by individuals that could previously replicate independently, cooperating to form a new, more complex life form. For example, archaea and eubacteria formed eukaryotic cells, and cells formed multicellular organisms. However, not all cooperative groups are en route to major transitions. How can we explain why major evolutionary transitions have or haven't taken place on different branches of the tree of life? We break down major transitions into two steps: the formation of a cooperative group and the transformation of that group into an integrated entity. We show how these steps require cooperation, division of labor, communication, mutual dependence, and negligible within-group conflict. We find that certain ecological conditions and the ways in which groups form have played recurrent roles in driving multiple transitions. In contrast, we find that other factors have played relatively minor roles at many key points, such as within-group kin discrimination and mechanisms to actively repress competition. More generally, by identifying the small number of factors that have driven major transitions, we provide a simpler and more unified description of how life on earth has evolved.T he evolution of life, from simple organic compounds in a primordial soup to the amazing diversity of contemporary organisms, has taken roughly 3.5 billion years. How can we explain the evolution of increasingly complex organisms over this period? A traditional approach has been to consider the succession of taxonomic groups, such as the age of fishes giving rise to the age of amphibians, which gave way to the age of reptiles, and so on. Although this approach has some uses, it is biased toward relatively large plants and animals and lacks a conceptual or predictive framework, in that it suggests we look for different explanations for each succession (1).Twenty years ago, Maynard Smith and Szathmáry (2) revolutionized our understanding of life on earth by showing how the key steps in the evolution of life on earth had been driven by a small number of "major evolutionary transitions." In each transition, a group of individuals that could previously replicate independently cooperate to form a new, more complex life form. For example, genes cooperated to form genomes, archaea and eubacteria formed eukaryotic cells, and cells cooperated to form multicellular organisms (Table 1).The major transitions approach provides a conceptual framework that facilitates comparison across pivotal moments in the history of life (2, 3). It suggests that the same problem arises at each transition: How are the potentially selfish interests of individuals overcome to form mutually dependent cooperative groups? We can then ask whether there are any similarities across transitions in the answers to this problem. Consequently, rather than looking for different explanations for the succession of different taxonomic groups, we ...

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Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies

Cited by 404 publications

References 113 publications

Taxonomy, Physiology, and Natural Products of Actinobacteria

Taxonomy, Physiology, and Natural Products of Actinobacteria

Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence

Major evolutionary transitions in individuality

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