Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts

ABSTRACT While fastidious microbes can be abundant and ubiquitous in their natural communities, many fail to grow axenically in laboratories due to auxotrophies or other dependencies. To overcome auxotrophies, these microbes rely on their surrounding cohort. A cohort may consist of kin (ecotypes) or...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Rhiannon Mondav, Stefan Bertilsson, Moritz Buck, Silke Langenheder, Eva S. Lindström, Sarahi L. Garcia
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Actinobacteria alphaproteobacteria aquatic bacterioplankton common goods ecology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a854b575a2794f8ca55ad42c73af9a29
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:a854b575a2794f8ca55ad42c73af9a29
record_format	dspace
spelling	oai:doaj.org-article:a854b575a2794f8ca55ad42c73af9a292021-12-02T18:44:36ZStreamlined and Abundant Bacterioplankton Thrive in Functional Cohorts10.1128/mSystems.00316-202379-5077https://doaj.org/article/a854b575a2794f8ca55ad42c73af9a292020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00316-20https://doaj.org/toc/2379-5077ABSTRACT While fastidious microbes can be abundant and ubiquitous in their natural communities, many fail to grow axenically in laboratories due to auxotrophies or other dependencies. To overcome auxotrophies, these microbes rely on their surrounding cohort. A cohort may consist of kin (ecotypes) or more distantly related organisms (community) with the cooperation being reciprocal or nonreciprocal and expensive (Black Queen hypothesis) or costless (by-product). These metabolic partnerships (whether at single species population or community level) enable dominance by and coexistence of these lineages in nature. Here we examine the relevance of these cooperation models to explain the abundance and ubiquity of the dominant fastidious bacterioplankton of a dimictic mesotrophic freshwater lake. Using both culture-dependent (dilution mixed cultures) and culture-independent (small subunit [SSU] rRNA gene time series and environmental metagenomics) methods, we independently identified the primary cohorts of actinobacterial genera “Candidatus Planktophila” (acI-A) and “Candidatus Nanopelagicus” (acI-B) and the proteobacterial genus “Candidatus Fonsibacter” (LD12). While “Ca. Planktophila” and “Ca. Fonsibacter” had no correlation in their natural habitat, they have the potential to be complementary in laboratory settings. We also investigated the bifunctional catalase-peroxidase enzyme KatG (a common good which “Ca. Planktophila” is dependent upon) and its most likely providers in the lake. Further, we found that while ecotype and community cooperation combined may explain “Ca. Planktophila” population abundance, the success of “Ca. Nanopelagicus” and “Ca. Fonsibacter” is better explained as a community by-product. Ecotype differentiation of “Ca. Fonsibacter” as a means of escaping predation was supported but not for overcoming auxotrophies. IMPORTANCE This study examines evolutionary and ecological relationships of three of the most ubiquitous and abundant freshwater bacterial genera: “Ca. Planktophila” (acI-A), “Ca. Nanopelagicus” (acI-B), and “Ca. Fonsibacter” (LD12). Due to high abundance, these genera might have a significant influence on nutrient cycling in freshwaters worldwide, and this study adds a layer of understanding to how seemingly competing clades of bacteria can coexist by having different cooperation strategies. Our synthesis ties together network and ecological theory with empirical evidence and lays out a framework for how the functioning of populations within complex microbial communities can be studied.Rhiannon MondavStefan BertilssonMoritz BuckSilke LangenhederEva S. LindströmSarahi L. GarciaAmerican Society for MicrobiologyarticleActinobacteriaalphaproteobacteriaaquaticbacterioplanktoncommon goodsecologyMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Actinobacteria alphaproteobacteria aquatic bacterioplankton common goods ecology Microbiology QR1-502
spellingShingle	Actinobacteria alphaproteobacteria aquatic bacterioplankton common goods ecology Microbiology QR1-502 Rhiannon Mondav Stefan Bertilsson Moritz Buck Silke Langenheder Eva S. Lindström Sarahi L. Garcia Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts
description	ABSTRACT While fastidious microbes can be abundant and ubiquitous in their natural communities, many fail to grow axenically in laboratories due to auxotrophies or other dependencies. To overcome auxotrophies, these microbes rely on their surrounding cohort. A cohort may consist of kin (ecotypes) or more distantly related organisms (community) with the cooperation being reciprocal or nonreciprocal and expensive (Black Queen hypothesis) or costless (by-product). These metabolic partnerships (whether at single species population or community level) enable dominance by and coexistence of these lineages in nature. Here we examine the relevance of these cooperation models to explain the abundance and ubiquity of the dominant fastidious bacterioplankton of a dimictic mesotrophic freshwater lake. Using both culture-dependent (dilution mixed cultures) and culture-independent (small subunit [SSU] rRNA gene time series and environmental metagenomics) methods, we independently identified the primary cohorts of actinobacterial genera “Candidatus Planktophila” (acI-A) and “Candidatus Nanopelagicus” (acI-B) and the proteobacterial genus “Candidatus Fonsibacter” (LD12). While “Ca. Planktophila” and “Ca. Fonsibacter” had no correlation in their natural habitat, they have the potential to be complementary in laboratory settings. We also investigated the bifunctional catalase-peroxidase enzyme KatG (a common good which “Ca. Planktophila” is dependent upon) and its most likely providers in the lake. Further, we found that while ecotype and community cooperation combined may explain “Ca. Planktophila” population abundance, the success of “Ca. Nanopelagicus” and “Ca. Fonsibacter” is better explained as a community by-product. Ecotype differentiation of “Ca. Fonsibacter” as a means of escaping predation was supported but not for overcoming auxotrophies. IMPORTANCE This study examines evolutionary and ecological relationships of three of the most ubiquitous and abundant freshwater bacterial genera: “Ca. Planktophila” (acI-A), “Ca. Nanopelagicus” (acI-B), and “Ca. Fonsibacter” (LD12). Due to high abundance, these genera might have a significant influence on nutrient cycling in freshwaters worldwide, and this study adds a layer of understanding to how seemingly competing clades of bacteria can coexist by having different cooperation strategies. Our synthesis ties together network and ecological theory with empirical evidence and lays out a framework for how the functioning of populations within complex microbial communities can be studied.
format	article
author	Rhiannon Mondav Stefan Bertilsson Moritz Buck Silke Langenheder Eva S. Lindström Sarahi L. Garcia
author_facet	Rhiannon Mondav Stefan Bertilsson Moritz Buck Silke Langenheder Eva S. Lindström Sarahi L. Garcia
author_sort	Rhiannon Mondav
title	Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts
title_short	Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts
title_full	Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts
title_fullStr	Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts
title_full_unstemmed	Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts
title_sort	streamlined and abundant bacterioplankton thrive in functional cohorts
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/a854b575a2794f8ca55ad42c73af9a29
work_keys_str_mv	AT rhiannonmondav streamlinedandabundantbacterioplanktonthriveinfunctionalcohorts AT stefanbertilsson streamlinedandabundantbacterioplanktonthriveinfunctionalcohorts AT moritzbuck streamlinedandabundantbacterioplanktonthriveinfunctionalcohorts AT silkelangenheder streamlinedandabundantbacterioplanktonthriveinfunctionalcohorts AT evaslindstrom streamlinedandabundantbacterioplanktonthriveinfunctionalcohorts AT sarahilgarcia streamlinedandabundantbacterioplanktonthriveinfunctionalcohorts
_version_	1718377756497018880

Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts

Ejemplares similares