Understanding Microbial Divisions of Labor

Zhang, Zheren; Claessen, Dennis; Rozen, Daniel E.

doi:10.3389/fmicb.2016.02070

Cited by 47 publications

(36 citation statements)

References 77 publications

(127 reference statements)

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“…Nevertheless, it has been documented that individuals of low genetic relatedness can help each other, as long as they share a locus encoding for cooperation or a mechanism exists that allows discrimination against non-cooperators [2][3][4][5] . Cooperation may also take place via division of labour between (sub)populations of cells carrying/expressing different cooperative loci [6][7][8] .…”

Section: Introductionmentioning

confidence: 99%

Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms

et al. 2018

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Closely related microbes often cooperate, but the prevalence and stability of cooperation between different genotypes remains debatable. Here, we track the evolution of pellicle biofilms formed through genetic division of labour and ask whether partially deficient partners can evolve autonomy.Pellicles of Bacillus subtilis rely on an extracellular matrix composed of exopolysaccharide (EPS) and the fibre protein TasA. In monocultures, ∆eps and ∆tasA mutants fail to form pellicles, but, facilitated by cooperation, they succeed in co-culture. Interestingly, cooperation collapses on an evolutionary timescale, and ∆tasA gradually outcompetes its partner ∆eps. Pellicle formation can evolve independently from division of labour in ∆eps and ∆tasA monocultures, by selection acting on the residual matrix component, TasA or EPS respectively. Using a set of interdisciplinary tools, we unravel that the TasA-producer (∆eps) evolves via an unconventional but reproducible substitution in TasA that modulates the biochemical properties of the protein. On the contrary, the EPS-producer (ΔtasA) undergoes genetically variable adaptations, all leading to enhanced EPS secretion and biofilms with different biomechanical properties. Finally, we revisit the collapse of division of labour between Δeps and ΔtasA in light of a strong frequency vs. exploitability trade-off that manifested in the solitarily evolving partners. We propose such trade-off differences may represent an additional barrier to evolution of division of labour between genetically distinct microbes.

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Section: Introductionmentioning

confidence: 99%

Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms

et al. 2018

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“…Evidence is accumulating that, like eukaryotes, bacteria undergo a process of programmed cell death (PCD). Bacterial multicellularity implies a lifestyle involving cellular heterogeneity and the occasional sacrifice of selected cells for the benefit of survival of the colony (70–72). PCD is likely a major hallmark of multicellularity (8), and has been described in the biofilm-film forming Streptococcus (14) and Bacillus (10), in Myxobacteria that form fruiting bodies (59), in the filamentous cyanobacteria (3, 40), and in the branching Streptomyces (35, 38, 61).…”

Section: Resultsmentioning

confidence: 99%

High-resolution analysis of the peptidoglycan composition inStreptomyces coelicolor

Wezel

Aart

Spijksma

et al. 2018

Preprint

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22The bacterial cell wall maintains cell shape and protects against bursting by the 23 turgor. A major constituent of the cell wall is peptidoglycan (PG), which is 24 continuously modified to allow cell growth and differentiation through the concerted 25 activity of biosynthetic and hydrolytic enzymes. Streptomycetes are Gram-positive 26 bacteria with a complex multicellular life style alternating between mycelial growth 27 and the formation of reproductive spores. This involves cell-wall remodeling at apical 28 sites of the hyphae during cell elongation and autolytic degradation of the vegetative 29 mycelium during the onset of development and antibiotic production. Here, we show 30 that there are distinct differences in the cross-linking and maturation of the PG 31 between exponentially growing vegetative hyphae and the aerial hyphae that 32 undergo sporulation. LC-MS/MS analysis identified over 80 different muropeptides, 33 revealing that major PG hydrolysis takes place over the course of mycelial growth. 34 Half of the dimers lack one of the disaccharide units in transition-phase cells, most 35 likely due to autolytic activity. De-acetylation of MurNAc to MurN was particularly 36 pronounced in spores, suggesting that MurN plays a role in spore development. 37 Taken together, our work highlights dynamic and growth phase-dependent 38 construction and remodeling of PG in Streptomyces. 39 40 IMPORTANCE 41 Streptomycetes are bacteria with a complex lifestyle, which are model organisms for 42 bacterial multicellularity. From a single spore a large multigenomic, multicellular 43 mycelium is formed, which differentiates to form spores. Programmed cell death is an 44 important event during the onset of morphological differentiation. In this work we 45 3 provide new insights into the changes in the peptidoglycan architecture over time, 46 highlighting changes over the course of development and between growing mycelia 47 56 Peptidoglycan (PG) is a major component of the bacterial cell wall. It forms a physical 57boundary that maintains cell shape, protects cellular integrity against the osmotic 58 pressure and acts as a scaffold for large protein assemblies and exopolymers (66). 59The cell wall is a highly dynamic macromolecule that is continuously constructed and 60 deconstructed to allow for cell growth and to meet environmental demands (27). PG 61 is built up of glycan strands of alternating N-acetylglucosamine (GlcNAc) and N-62 acetylmuramic acid (MurNAc) residues that are connected by short peptides to form 63 a mesh-like polymer. PG biosynthesis starts with the synthesis of PG precursors by 64 the Mur enzymes in the cytoplasm and cell membrane, resulting in lipid II precursor, 65 undecaprenylpyrophosphoryl-MurNAc(GlcNAc)-pentapeptide. Lipid II is transported 66 across the cell membrane by MurJ and/or FtsW/SEDS proteins and the PG is 67 polymerized and incorporated into the existing cell wall by the activities of 68 glycosyltransferases and transpeptidases (9, 30, 57). 69 The Gram-positive model bacterium Bacillus ...

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“…First, Streptomyces colonies emerge from a single spore and are clonal 19 . This, together with their filamentous mode-of-growth, ensures that costly individual traits can be maintained due to their indirect fitness benefits 4, 5, 13 . And because resistance to the diversified antibiotic profile of mutant strains is unlikely to be present in competing strains, only the parent strain stands to benefit from their sacrifice.…”

Section: Discussionmentioning

confidence: 99%

Antibiotic production is organized by a division of labour inStreptomyces

Zhang

Barsy

Liem

et al. 2019

Preprint

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26One of the hallmark behaviors of social groups is division of labour, where different group members 27 become specialized to carry out complementary tasks. By dividing labour, cooperative groups of 28 individuals increase their efficiency, thereby raising group fitness even if these specialized behaviors 29reduce the fitness of individual group members. Here we provide evidence that antibiotic production 30 in colonies of the multicellular bacterium Streptomyces coelicolor is coordinated by a division of labour. 31We show that S. coelicolor colonies are genetically heterogeneous due to massive amplifications and 32 deletions to the chromosome. Cells with gross chromosomal changes produce an increased diversity 33 of secondary metabolites and secrete significantly more antibiotics; however, these changes come at 34 the cost of dramatically reduced individual fitness, providing direct evidence for a trade-off between 35 secondary metabolite production and fitness. Finally, we show that colonies containing mixtures of 36 mutant strains and their parents produce significantly more antibiotics, while colony-wide spore 37 production remains unchanged. Our work demonstrates that by generating mutants that are 38 specialized to hyper-produce antibiotics, streptomycetes reduce the colony-wide fitness costs of 39 secreted secondary metabolites while maximizing the yield and diversity of these products. 40

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Understanding Microbial Divisions of Labor

Cited by 47 publications

References 77 publications

Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms

Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms

High-resolution analysis of the peptidoglycan composition inStreptomyces coelicolor

Antibiotic production is organized by a division of labour inStreptomyces

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