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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“…For example, oligosaccharide exploiters, which grow on hydrolysis products but do produce hydrolases (a.k.a "cheaters"), have been shown to invade chitin degrading communities in the ocean, competing for carbon with degraders and reducing their yield (Pollak et al, 2021). Both degraders and exploiters release amino acids and TCA cycle intermediates such as malate or succinate (Enke et al, 2019;Pontrelli et al, 2021) that fuel the growth of scavengers specialized on consuming these metabolites. Likewise, during fucoidan degradation, fucose is partially respired and fermented into large amounts of lactate and propanediol (Sichert et al, 2020), which is likely consumed by neighboring microbes.…”

Section: Challenge 5 | Impact Of Microbial Interactions On Hydrolysis Ratesmentioning

confidence: 99%

Polysaccharide-Bacteria Interactions From the Lens of Evolutionary Ecology

Sichert

Cordero

2021

Front. Microbiol.

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Microbes have the unique ability to break down the complex polysaccharides that make up the bulk of organic matter, initiating a cascade of events that leads to their recycling. Traditionally, the rate of organic matter degradation is perceived to be limited by the chemical and physical structure of polymers. Recent advances in microbial ecology, however, suggest that polysaccharide persistence can result from non-linear growth dynamics created by the coexistence of alternate degradation strategies, metabolic roles as well as by ecological interactions between microbes. This complex “landscape” of degradation strategies and interspecific interactions present in natural microbial communities appears to be far from evolutionarily stable, as frequent gene gain and loss reshape enzymatic repertoires and metabolic roles. In this perspective, we discuss six challenges at the heart of this problem, ranging from the evolution of genetic repertoires, phenotypic heterogeneity in clonal populations, the development of a trait-based ecology, and the impact of metabolic interactions and microbial cooperation on degradation rates. We aim to reframe some of the key questions in the study of polysaccharide-bacteria interactions in the context of eco-evolutionary dynamics, highlighting possible research directions that, if pursued, would advance our understanding of polysaccharide degraders at the interface between biochemistry, ecology and evolution.

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Section: Challenge 5 | Impact Of Microbial Interactions On Hydrolysis Ratesmentioning

confidence: 99%

Polysaccharide-Bacteria Interactions From the Lens of Evolutionary Ecology

Sichert

Cordero

2021

Front. Microbiol.

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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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“…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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Hierarchical control of microbial community assembly

Cited by 8 publications

References 59 publications

Polysaccharide-Bacteria Interactions From the Lens of Evolutionary Ecology

Polysaccharide-Bacteria Interactions From the Lens of Evolutionary Ecology

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

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