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Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles

Particulate organic matter (POM) in the ocean sustains diverse communities of bacteria that mediate the remineralization of organic complex matter. However, the variability of these particles and of the environmental conditions surrounding them present a challenge to the study of the ecological proc...

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Autores principales: Pascual-García, Alberto, Schwartzman, Julia, Enke, Tim N., Iffland-Stettner, Arion, Cordero, Otto X., Bonhoeffer, Sebastian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9260654/
https://www.ncbi.nlm.nih.gov/pubmed/35814698
http://dx.doi.org/10.3389/fmicb.2022.812116
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author Pascual-García, Alberto
Schwartzman, Julia
Enke, Tim N.
Iffland-Stettner, Arion
Cordero, Otto X.
Bonhoeffer, Sebastian
author_facet Pascual-García, Alberto
Schwartzman, Julia
Enke, Tim N.
Iffland-Stettner, Arion
Cordero, Otto X.
Bonhoeffer, Sebastian
author_sort Pascual-García, Alberto
collection PubMed
description Particulate organic matter (POM) in the ocean sustains diverse communities of bacteria that mediate the remineralization of organic complex matter. However, the variability of these particles and of the environmental conditions surrounding them present a challenge to the study of the ecological processes shaping particle-associated communities and their function. In this work, we utilize data from experiments in which coastal water communities are grown on synthetic particles to ask which are the most important ecological drivers of their assembly and associated traits. Combining 16S rRNA amplicon sequencing with shotgun metagenomics, together with an analysis of the full genomes of a subset of isolated strains, we were able to identify two-to-three distinct community classes, corresponding to early vs. late colonizers. We show that these classes are shaped by environmental selection (early colonizers) and facilitation (late colonizers) and find distinctive traits associated with each class. While early colonizers have a larger proportion of genes related to the uptake of nutrients, motility, and environmental sensing with few pathways enriched for metabolism, late colonizers devote a higher proportion of genes for metabolism, comprising a wide array of different pathways including the metabolism of carbohydrates, amino acids, and xenobiotics. Analysis of selected pathways suggests the existence of a trophic-chain topology connecting both classes for nitrogen metabolism, potential exchange of branched chain amino acids for late colonizers, and differences in bacterial doubling times throughout the succession. The interpretation of these traits suggests a distinction between early and late colonizers analogous to other classifications found in the literature, and we discuss connections with the classical distinction between r- and K-strategists.
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spelling pubmed-92606542022-07-08 Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles Pascual-García, Alberto Schwartzman, Julia Enke, Tim N. Iffland-Stettner, Arion Cordero, Otto X. Bonhoeffer, Sebastian Front Microbiol Microbiology Particulate organic matter (POM) in the ocean sustains diverse communities of bacteria that mediate the remineralization of organic complex matter. However, the variability of these particles and of the environmental conditions surrounding them present a challenge to the study of the ecological processes shaping particle-associated communities and their function. In this work, we utilize data from experiments in which coastal water communities are grown on synthetic particles to ask which are the most important ecological drivers of their assembly and associated traits. Combining 16S rRNA amplicon sequencing with shotgun metagenomics, together with an analysis of the full genomes of a subset of isolated strains, we were able to identify two-to-three distinct community classes, corresponding to early vs. late colonizers. We show that these classes are shaped by environmental selection (early colonizers) and facilitation (late colonizers) and find distinctive traits associated with each class. While early colonizers have a larger proportion of genes related to the uptake of nutrients, motility, and environmental sensing with few pathways enriched for metabolism, late colonizers devote a higher proportion of genes for metabolism, comprising a wide array of different pathways including the metabolism of carbohydrates, amino acids, and xenobiotics. Analysis of selected pathways suggests the existence of a trophic-chain topology connecting both classes for nitrogen metabolism, potential exchange of branched chain amino acids for late colonizers, and differences in bacterial doubling times throughout the succession. The interpretation of these traits suggests a distinction between early and late colonizers analogous to other classifications found in the literature, and we discuss connections with the classical distinction between r- and K-strategists. Frontiers Media S.A. 2022-06-23 /pmc/articles/PMC9260654/ /pubmed/35814698 http://dx.doi.org/10.3389/fmicb.2022.812116 Text en Copyright © 2022 Pascual-García, Schwartzman, Enke, Iffland-Stettner, Cordero and Bonhoeffer. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Pascual-García, Alberto
Schwartzman, Julia
Enke, Tim N.
Iffland-Stettner, Arion
Cordero, Otto X.
Bonhoeffer, Sebastian
Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles
title Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles
title_full Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles
title_fullStr Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles
title_full_unstemmed Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles
title_short Turnover in Life-Strategies Recapitulates Marine Microbial Succession Colonizing Model Particles
title_sort turnover in life-strategies recapitulates marine microbial succession colonizing model particles
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9260654/
https://www.ncbi.nlm.nih.gov/pubmed/35814698
http://dx.doi.org/10.3389/fmicb.2022.812116
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