Hierarchical control of microbial community assembly

Pontrelli, Sammy; Szabo, Rachel E.; Pollak, Shaul; Schwartzman, Julia; Ledezma-Tejeida, Daniela; Ox, Cordero; Sauer, Uwe

doi:10.1101/2021.06.22.449372

Cited by 8 publications

(6 citation statements)

References 59 publications

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“…In contrast, strains that have increased enzymatic secretions can breakdown polysaccharides by adopting dispersed growth modes, that can facilitate migration of cells to new polysaccharide particles in nature. Additionally, in communities where multiple strains coexist 4,5,15,24 , the degradative activity of high enzyme secretors can create public goods that can positively influence the growth of not only the low enzyme producers but also strains that lack the ability to degrade polysaccharides and rely on cross-feeding of monomers from the polymer degraders 13,25,26 .…”

Section: Resultsmentioning

confidence: 99%

Intercellular collectivity is governed by enzyme secretion strategies in marine polysaccharide degrading bacteria

D’Souza

Ebrahimi

Stubbusch

et al. 2022

Preprint

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Polysaccharide breakdown by bacteria requires the activity of enzymes that degrade polymers extracellularly. This generates a localized pool of breakdown products that are accessible to the enzyme producers themselves as well as to other organisms. Marine bacterial taxa often show marked differences in the production and secretion of degradative enzymes that break down polysaccharides. These differences can have profound effects on the pool of diffusible breakdown products and hence on the ecological dynamics. However, the consequences of differences in enzymatic secretions on cellular growth dynamics and interactions are unclear. Here we combine experiments and models to study the growth dynamics of single cells within populations of marine Vibrionaceae strains that grow on the abundant marine polymer alginate, using microfluidics coupled to quantitative single-cell analysis and mathematical modelling. We find that strains that have low extracellular secretions of alginate lyases show stronger aggregative behaviors compared to strains that secrete high levels of enzymes. One plausible reason for this observation is that low secretors require a higher cellular density to achieve maximal growth rates in comparison with high secretors. Our findings indicate that increased aggregation increases intercellular synergy amongst cells of low-secreting strains. By mathematically modelling the impact of the level of degradative enzyme secretion on the rate of oligomer loss to diffusion, we find that enzymatic capability modulates the propensity of cells within clonal populations to cooperate or compete with each other. Our experiments and models demonstrate that marine bacteria display distinct aggregative behaviors and intercellular interactions based on their enzymatic secretion capabilities when growing on polysaccharides.

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Section: Resultsmentioning

confidence: 99%

Intercellular collectivity is governed by enzyme secretion strategies in marine polysaccharide degrading bacteria

D’Souza

Ebrahimi

Stubbusch

et al. 2022

Preprint

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“…The difference in length of growth phase can be explained by different metabolic niches: while marine polymer degraders tend to be highly specialized for the polymers they cleave, cross-feeders exhibit a wider metabolic niche (29). Being a generalist for metabolic by-products allows the cross-feeders to grow on various metabolites released by degrader during growth on the polymer (30).…”

Section: Resultsmentioning

confidence: 99%

Changes in interactions over ecological time scales influence single cell growth dynamics in a metabolically coupled marine microbial community

Daniels

Vliet

Ackermann

2022

Preprint

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Microbial communities thrive in almost all habitats on earth. Within these communities, cells interact through the release and uptake of metabolites. These interactions can have synergistic or antagonistic effects on individual community members. The collective metabolic activity of microbial communities leads to changes in their local environment. As the environment changes over time, the nature of the interactions between cells can change. We currently lack understanding of how such dynamic feedbacks affect the growth dynamics of individual microbes and of the community as a whole. Here we study how interactions mediated by the exchange of metabolites through the environment change over time within a simple marine microbial community. We used a microfluidic-based approach that allows us to disentangle the effect cells have on their environment from how they respond to their environment. We found that the interactions between two species - a degrader of chitin and a cross-feeder that consumes metabolic by-products - changes dynamically over time as cells modify their environment. Cells initially interact positively and then start to compete at later stages of growth. Our results demonstrate that interactions between microbes are not static and depend on the state of the environment, emphasizing the importance of disentangling how modifications of the environment affects species interactions. This experimental approach can shed new light on how interspecies interactions scale up to community level processes in natural environments.

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“…The particles were initially colonized by bacteria, and later by flagellates. Cordero et al have taken a similar approach to understand colonization dynamics (Datta et al, 2016;Ebrahimi et al, 2019;Enke et al, 2019;Pontrelli et al, 2021). These studies shed light on the metabolic roles played by different players during particle colonization dynamics: primary degraders excrete enzymes to break down polysaccharide chains, which creates a niche for secondary degraders capable of consuming monomers and oligomers of the polysaccharide, which in turn makes way for scavengers that take up metabolic byproducts of the primary and secondary degraders (ammonia, amino acids).…”

Section: Marine Snowmentioning

confidence: 99%

An ensemble approach to the structure-function problem in microbial communities

et al. 2022

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The metabolic activity of microbial communities plays a primary role in the flow of essential nutrients throughout the biosphere. Molecular genetics has revealed the metabolic pathways that model organisms utilize to generate energy and biomass, but we understand little about how the metabolism of diverse, natural communities emerges from the collective action of its constituents. We propose that quantifying and mapping metabolic fluxes to sequencing measurements of genomic, taxonomic, or transcriptional variation across an ensemble of diverse communities, either in the laboratory or in the wild, can reveal low-dimensional descriptions of community structure that can explain or predict their emergent metabolic activity. We survey the types of communities for which this approach might be best suited, review the analytical techniques available for quantifying metabolite fluxes in communities, and discuss what types of data analysis approaches might be lucrative for learning the structure-function mapping in communities from these data.

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Hierarchical control of microbial community assembly

Cited by 8 publications

References 59 publications

Intercellular collectivity is governed by enzyme secretion strategies in marine polysaccharide degrading bacteria

Intercellular collectivity is governed by enzyme secretion strategies in marine polysaccharide degrading bacteria

Changes in interactions over ecological time scales influence single cell growth dynamics in a metabolically coupled marine microbial community

An ensemble approach to the structure-function problem in microbial communities

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