Spatial organization in microbial range expansion emerges from trophic dependencies and successful lineages

Borer, Benedict; Ciccarese, Davide; Johnson, David R.; Or, Dani

doi:10.1038/s42003-020-01409-y

Cited by 42 publications

(47 citation statements)

References 65 publications

(83 reference statements)

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“…Another example of an environmental effect involves two mutants of Pseudomonas stuzeri. Depending on the pH, the mutants can shift from competition to strong cross-feeding of nitrite, which is a toxic compound at low pH (Borer et al, 2020).…”

Section: Mechanisms Behind Cross-feedingmentioning

confidence: 99%

Microbial Systems Ecology to Understand Cross-Feeding in Microbiomes

et al. 2021

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Understanding how microorganism-microorganism interactions shape microbial assemblages is a key to deciphering the evolution of dependencies and co-existence in complex microbiomes. Metabolic dependencies in cross-feeding exist in microbial communities and can at least partially determine microbial community composition. To parry the complexity and experimental limitations caused by the large number of possible interactions, new concepts from systems biology aim to decipher how the components of a system interact with each other. The idea that cross-feeding does impact microbiome assemblages has developed both theoretically and empirically, following a systems biology framework applied to microbial communities, formalized as microbial systems ecology (MSE) and relying on integrated-omics data. This framework merges cellular and community scales and offers new avenues to untangle microbial coexistence primarily by metabolic modeling, one of the main approaches used for mechanistic studies. In this mini-review, we first give a concise explanation of microbial cross-feeding. We then discuss how MSE can enable progress in microbial research. Finally, we provide an overview of a MSE framework mostly based on genome-scale metabolic-network reconstruction that combines top-down and bottom-up approaches to assess the molecular mechanisms of deterministic processes of microbial community assembly that is particularly suitable for use in synthetic biology and microbiome engineering.

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Section: Mechanisms Behind Cross-feedingmentioning

confidence: 99%

Microbial Systems Ecology to Understand Cross-Feeding in Microbiomes

et al. 2021

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“…Laboratory and in silico experiments demonstrated that stochastic processes [ 32 , 36 ] and mechanical forces acting between cells [ 42 , 43 ] in combination with initial spatial positioning [ 24 , 36 ] can control the dynamics of diversity loss during sessile microbial range expansion. Further investigations demonstrated the importance of initial spatial positioning when sustained by the local substrate landscape, thus leading to the establishment of successful lineages at the expansion edge [ 44 ]. In other words, the presence of a specific cell-type at the expansion edge may result from stochastic processes that do not require beneficial mutations.…”

Section: Introductionmentioning

confidence: 99%

Rare and localized events stabilize microbial community composition and patterns of spatial self-organization in a fluctuating environment

et al. 2022

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Spatial self-organization is a hallmark of surface-associated microbial communities that is governed by local environmental conditions and further modified by interspecific interactions. Here, we hypothesize that spatial patterns of microbial cell-types can stabilize the composition of cross-feeding microbial communities under fluctuating environmental conditions. We tested this hypothesis by studying the growth and spatial self-organization of microbial co-cultures consisting of two metabolically interacting strains of the bacterium Pseudomonas stutzeri. We inoculated the co-cultures onto agar surfaces and allowed them to expand (i.e. range expansion) while fluctuating environmental conditions that alter the dependency between the two strains. We alternated between anoxic conditions that induce a mutualistic interaction and oxic conditions that induce a competitive interaction. We observed co-occurrence of both strains in rare and highly localized clusters (referred to as “spatial jackpot events”) that persist during environmental fluctuations. To resolve the underlying mechanisms for the emergence of spatial jackpot events, we used a mechanistic agent-based mathematical model that resolves growth and dispersal at the scale relevant to individual cells. While co-culture composition varied with the strength of the mutualistic interaction and across environmental fluctuations, the model provides insights into the formation of spatially resolved substrate landscapes with localized niches that support the co-occurrence of the two strains and secure co-culture function. This study highlights that in addition to spatial patterns that emerge in response to environmental fluctuations, localized spatial jackpot events ensure persistence of strains across dynamic conditions.

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“…This expectation, however, is not always realized. We analyzed patterns of spatial self-organization that emerged as a synthetic two-strain cross-feeding community expanded across an initial environment that was spatially homogeneous [ 18 , 20 , 37 ] (Fig. 1 ).…”

Section: Introductionmentioning

confidence: 99%

Causes and consequences of pattern diversification in a spatially self-organizing microbial community

2021

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Surface-attached microbial communities constitute a vast amount of life on our planet. They contribute to all major biogeochemical cycles, provide essential services to our society and environment, and have important effects on human health and disease. They typically consist of different interacting genotypes that arrange themselves non-randomly across space (referred to hereafter as spatial self-organization). While spatial self-organization is important for the functioning, ecology, and evolution of these communities, the underlying determinants of spatial self-organization remain unclear. Here, we performed a combination of experiments, statistical modeling, and mathematical simulations with a synthetic cross-feeding microbial community consisting of two isogenic strains. We found that two different patterns of spatial self-organization emerged at the same length and time scales, thus demonstrating pattern diversification. This pattern diversification was not caused by initial environmental heterogeneity or by genetic heterogeneity within populations. Instead, it was caused by nongenetic heterogeneity within populations, and we provide evidence that the source of this nongenetic heterogeneity is local differences in the initial spatial positionings of individuals. We further demonstrate that the different patterns exhibit different community-level properties; namely, they have different expansion speeds. Together, our results demonstrate that pattern diversification can emerge in the absence of initial environmental heterogeneity or genetic heterogeneity within populations and can affect community-level properties, thus providing novel insights into the causes and consequences of microbial spatial self-organization.

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Spatial organization in microbial range expansion emerges from trophic dependencies and successful lineages

Cited by 42 publications

References 65 publications

Microbial Systems Ecology to Understand Cross-Feeding in Microbiomes

Microbial Systems Ecology to Understand Cross-Feeding in Microbiomes

Rare and localized events stabilize microbial community composition and patterns of spatial self-organization in a fluctuating environment

Causes and consequences of pattern diversification in a spatially self-organizing microbial community

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