Interspecies interactions that result in<i>Bacillus subtilis</i>forming biofilms are mediated mainly by members of its own genus

Shank, Elizabeth A.; Klepac‐Ceraj, Vanja; Collado‐Torres, Leonardo; Powers, Gordon E.; Losick, Richard; Kolter, Roberto

doi:10.1073/pnas.1103630108

Cited by 99 publications

(100 citation statements)

References 57 publications

(69 reference statements)

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“…At the cellular level, differential responses to these local environments [e.g., as gradients of gene expression (36) or position-dependent cell specialization (37)] may increase phenotypic variability and promote bacterial adaptation during infection (38). The gradients formed inside packed colonies may also be used by bacteria as a cue for positioning during biofilm development (39). In the case of P. aeruginosa, Pvd has been identified as a virulence factor in the development of infectious biofilms (28,(40)(41)(42) and confocal imaging has revealed that the Pvd pathway is not activated uniformly within biofilms (43,44).…”

Section: Discussionmentioning

confidence: 99%

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

Julou

Mora

Guillon

et al. 2013

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

132

160

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The maintenance of cooperation in populations where public goods are equally accessible to all but inflict a fitness cost on individual producers is a long-standing puzzle of evolutionary biology. An example of such a scenario is the secretion of siderophores by bacteria into their environment to fetch soluble iron. In a planktonic culture, these molecules diffuse rapidly, such that the same concentration is experienced by all bacteria. However, on solid substrates, bacteria form dense and packed colonies that may alter the diffusion dynamics through cell-cell contact interactions. In Pseudomonas aeruginosa microcolonies growing on solid substrate, we found that the concentration of pyoverdine, a secreted iron chelator, is heterogeneous, with a maximum at the center of the colony. We quantitatively explain the formation of this gradient by local exchange between contacting cells rather than by global diffusion of pyoverdine. In addition, we show that this local trafficking modulates the growth rate of individual cells. Taken together, these data provide a physical basis that explains the stability of public goods production in packed colonies.biofilm | evolution | noise | variability | ecology I ron is required for many enzymatic processes, and is therefore an essential nutrient. To overcome the low abundance of free iron in aerobic environments, bacteria, as well as other microorganisms, synthesize and secrete iron-chelating molecules called siderophores (1). Once released in the extracellular environment, siderophores diffuse and complex with iron. Because other bacteria can import them, siderophores can be regarded as public goods (2) and siderophore secretion is often cited as a model system for studying the stability of cooperation (3, 4). In this context, nonproducing mutants, which can enjoy the benefit of siderophores without bearing the cost of their production, have a selective advantage over the WT-producing strain and could, in principle, displace them on evolutionary time scales.This argument usually assumes that public good molecules are readily available to all, as is the case in planktonic cultures, where molecules diffuse freely and rapidly between cells. In liquid conditions, mutants that do not produce siderophores have, in fact, been shown to outcompete WT strains (5-8). However, the limited spatial dispersal of public goods can challenge this picture and has been proposed as a general mechanism for explaining the maintenance of cooperation (8-12). When dispersal is limited, public good molecules tend to stay in the vicinity of the producing subpopulations, allowing them to benefit preferentially from their own production, and thus to balance the advantage of opportunistic nonproducing strains. In many ecological situations, bacteria form complex, tightly packed, and spatially structured colonies, such as biofilms, where public good dispersal may be severely reduced compared with planktonic cultures. This raises the questions of how public good molecules circulate between cells in these natur...

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Section: Discussionmentioning

confidence: 99%

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

Julou

Mora

Guillon

et al. 2013

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

132

160

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“…In both B. subtilis and P. aeruginosa, the regulatory pathways of antimicrobial production are closely entangled with those of biofilm formation, because matrix and antimicrobial genes are coexpressed (252)(253)(254)(255)(256)(257)(258). In the case of B. subtilis, matrix production can be triggered by antimicrobials produced by competitors (104,106,107,137). In other words, B. subtilis cells likely cooperate to compete against other soildwelling organisms.…”

Section: Life Cycle Biology: the Ecology Of Cell Differentiationmentioning

confidence: 99%

“…These kinases sense a variety of environmental signals, including self-generated products like surfactin and matrix (105,(135)(136)(137)(138). Once phosphorylated, Spo0A∼P indirectly represses the expression of sinR (139)(140)(141).…”

Section: Regulation Of Differentiation In B Subtilismentioning

confidence: 99%

Division of Labor in Biofilms: the Ecology of Cell Differentiation

2015

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The dense aggregation of cells on a surface, as seen in biofilms, inevitably results in both environmental and cellular heterogeneity. For example, nutrient gradients can trigger cells to differentiate into various phenotypic states. Not only do cells adapt physiologically to the local environmental conditions, but they also differentiate into cell types that interact with each other. This allows for task differentiation and, hence, the division of labor. In this article, we focus on cell differentiation and the division of labor in three bacterial species: Myxococcus xanthus, Bacillus subtilis , and Pseudomonas aeruginosa . During biofilm formation each of these species differentiates into distinct cell types, in some cases leading to cooperative interactions. The division of labor and the cooperative interactions between cell types are assumed to yield an emergent ecological benefit. Yet in most cases the ecological benefits have yet to be elucidated. A notable exception is M. xanthus , in which cell differentiation within fruiting bodies facilitates the dispersal of spores. We argue that the ecological benefits of the division of labor might best be understood when we consider the dynamic nature of both biofilm formation and degradation.

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“…2-200 μm in diameter (Fig. 4 A−D), that bear a striking resemblance to microbial microcolonies, i.e., micrometer-scale clusters of physically adjacent microbial cells (42). Some inclusions show negative crystal shapes evidencing entrapment during crystal growth (Fig.…”

Section: Microfossil Inclusionsmentioning

confidence: 99%

Fluid mixing and the deep biosphere of a fossil Lost City-type hydrothermal system at the Iberia Margin

Klein

Humphris

Guo

et al. 2015

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

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Subseafloor mixing of reduced hydrothermal fluids with seawater is believed to provide the energy and substrates needed to support deep chemolithoautotrophic life in the hydrated oceanic mantle (i.e., serpentinite). However, geosphere-biosphere interactions in serpentinite-hosted subseafloor mixing zones remain poorly constrained. Here we examine fossil microbial communities and fluid mixing processes in the subseafloor of a Cretaceous Lost City-type hydrothermal system at the magma-poor passive Iberia Margin (Ocean Drilling Program Leg 149, Hole 897D). Brucite−calcite mineral assemblages precipitated from mixed fluids ca. 65 m below the Cretaceous paleo-seafloor at temperatures of 31.7 ± 4.3°C within steep chemical gradients between weathered, carbonate-rich serpentinite breccia and serpentinite. Mixing of oxidized seawater and strongly reducing hydrothermal fluid at moderate temperatures created conditions capable of supporting microbial activity. Dense microbial colonies are fossilized in brucite−calcite veins that are strongly enriched in organic carbon (up to 0.5 wt.% of the total carbon) but depleted in 13 C (δ 13 C TOC = −19.4‰). We detected a combination of bacterial diether lipid biomarkers, archaeol, and archaeal tetraethers analogous to those found in carbonate chimneys at the active Lost City hydrothermal field. The exposure of mantle rocks to seawater during the breakup of Pangaea fueled chemolithoautotrophic microbial communities at the Iberia Margin, possibly before the onset of seafloor spreading. Lost City-type serpentinization systems have been discovered at midocean ridges, in forearc settings of subduction zones, and at continental margins. It appears that, wherever they occur, they can support microbial life, even in deep subseafloor environments.serpentinization | microfossils | lipid biomarkers | brucite−calcite | passive margin

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Interspecies interactions that result inBacillus subtilisforming biofilms are mediated mainly by members of its own genus

Cited by 99 publications

References 57 publications

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

Division of Labor in Biofilms: the Ecology of Cell Differentiation

Fluid mixing and the deep biosphere of a fossil Lost City-type hydrothermal system at the Iberia Margin

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