Fine-scale diversity of microbial communities due to satellite niches in boom and bust environments
Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom and bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of stra...
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Published in | PLoS computational biology Vol. 18; no. 12; p. e1010244 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
01.12.2022
Public Library of Science (PLoS) |
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Online Access | Get full text |
ISSN | 1553-7358 1553-734X 1553-7358 |
DOI | 10.1371/journal.pcbi.1010244 |
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Abstract | Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom and bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of strains, but not more, have thus far remained unknown. Here, using a consumer-resource model of microbial ecosystems, we propose that by differentiating along Monod parameters characterizing microbial growth rates in high and low nutrient conditions, strains can coexist in patterns similar to those observed. In our model, boom and bust environments create satellite niches due to resource concentrations varying in time. These satellite niches can be occupied by closely related strains, thereby enabling their coexistence. We demonstrate that this result is valid even in complex environments consisting of multiple resources and species. In these complex communities, each species partitions resources differently and creates separate sets of satellite niches for their own strains. While there is no theoretical limit to the number of coexisting strains, in our simulations, we always find between 1 and 3 strains coexisting, consistent with known experiments and observations. |
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AbstractList | Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom and bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of strains, but not more, have thus far remained unknown. Here, using a consumer-resource model of microbial ecosystems, we propose that by differentiating along Monod parameters characterizing microbial growth rates in high and low nutrient conditions, strains can coexist in patterns similar to those observed. In our model, boom and bust environments create satellite niches due to resource concentrations varying in time. These satellite niches can be occupied by closely related strains, thereby enabling their coexistence. We demonstrate that this result is valid even in complex environments consisting of multiple resources and species. In these complex communities, each species partitions resources differently and creates separate sets of satellite niches for their own strains. While there is no theoretical limit to the number of coexisting strains, in our simulations, we always find between 1 and 3 strains coexisting, consistent with known experiments and observations. Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom and bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of strains, but not more, have thus far remained unknown. Here, using a consumer-resource model of microbial ecosystems, we propose that by differentiating along Monod parameters characterizing microbial growth rates in high and low nutrient conditions, strains can coexist in patterns similar to those observed. In our model, boom and bust environments create satellite niches due to resource concentrations varying in time. These satellite niches can be occupied by closely related strains, thereby enabling their coexistence. We demonstrate that this result is valid even in complex environments consisting of multiple resources and species. In these complex communities, each species partitions resources differently and creates separate sets of satellite niches for their own strains. While there is no theoretical limit to the number of coexisting strains, in our simulations, we always find between 1 and 3 strains coexisting, consistent with known experiments and observations. Recent genomic data have revealed the remarkable spectrum of microbial diversity in natural communities surrounding us, which harbor not only hundreds of species, but also a handful of closely related strains within each of those species (termed “oligo-colonization”). While the mechanisms behind species coexistence are much better studied, the mechanisms behind the coexistence of closely related strains have remained understudied. Here, using a simple consumer-resource model, we show that if strains differ on their Monod growth parameters, they can coexist even on a single limiting resource, provided that the environments, specifically resource concentrations, vary with time in boom and bust cycles. The Monod growth parameters describe how a strain’s growth rate changes with resource concentration, namely the half-maximal concentration and maximal growth rate. Simulations of our model show that both in simple and complex environments, even though an arbitrary number of strains can coexist, typically it is between 1 and 3 strains of a species that coexist over several randomly assembled communities, consistent with some experimental observations. This is because the allowed parameter space for coexistence shrinks significantly with the number of strains that coexist. Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom and bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of strains, but not more, have thus far remained unknown. Here, using a consumer-resource model of microbial ecosystems, we propose that by differentiating along Monod parameters characterizing microbial growth rates in high and low nutrient conditions, strains can coexist in patterns similar to those observed. In our model, boom and bust environments create satellite niches due to resource concentrations varying in time. These satellite niches can be occupied by closely related strains, thereby enabling their coexistence. We demonstrate that this result is valid even in complex environments consisting of multiple resources and species. In these complex communities, each species partitions resources differently and creates separate sets of satellite niches for their own strains. While there is no theoretical limit to the number of coexisting strains, in our simulations, we always find between 1 and 3 strains coexisting, consistent with known experiments and observations.Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom and bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of strains, but not more, have thus far remained unknown. Here, using a consumer-resource model of microbial ecosystems, we propose that by differentiating along Monod parameters characterizing microbial growth rates in high and low nutrient conditions, strains can coexist in patterns similar to those observed. In our model, boom and bust environments create satellite niches due to resource concentrations varying in time. These satellite niches can be occupied by closely related strains, thereby enabling their coexistence. We demonstrate that this result is valid even in complex environments consisting of multiple resources and species. In these complex communities, each species partitions resources differently and creates separate sets of satellite niches for their own strains. While there is no theoretical limit to the number of coexisting strains, in our simulations, we always find between 1 and 3 strains coexisting, consistent with known experiments and observations. |
Author | Goyal, Akshit Maslov, Sergei Fridman, Yulia Wang, Zihan |
AuthorAffiliation | 3 Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America 1 National Research Center “Kurchatov Institute”, Moscow, Russia Abdus Salam International Centre for Theoretical Physics, ITALY 4 Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America 2 Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America |
AuthorAffiliation_xml | – name: 1 National Research Center “Kurchatov Institute”, Moscow, Russia – name: 4 Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – name: 2 Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America – name: Abdus Salam International Centre for Theoretical Physics, ITALY – name: 3 Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America |
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Title | Fine-scale diversity of microbial communities due to satellite niches in boom and bust environments |
URI | https://www.ncbi.nlm.nih.gov/pubmed/36574450 https://www.proquest.com/docview/2758576654 https://pubmed.ncbi.nlm.nih.gov/PMC9829172 https://doaj.org/article/6961d16966944c7bb8261b94709c3051 |
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