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Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts

Mondav, Rhiannon and Bertilsson, Stefan and Buck, Moritz and Langenheder, Silke and Lindstrom, Eva S. and Garcia, Sarahi L. (2020). Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts. mSystems. 5 , e00316-20
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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.

Authors/Creators:Mondav, Rhiannon and Bertilsson, Stefan and Buck, Moritz and Langenheder, Silke and Lindstrom, Eva S. and Garcia, Sarahi L.
Title:Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts
Year of publishing :2020
Volume:5
Article number:e00316-20
Number of Pages:21
Publisher:AMER SOC MICROBIOLOGY
ISSN:2379-5077
Language:English
Publication Type:Journal article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Microbiology (Microbiology in the medical area to be 30109)
Keywords:Actinobacteria, alphaproteobacteria, aquatic, bacterioplankton, common goods, ecology, evolution, metagenomics, microbial communities, networks
URN:NBN:urn:nbn:se:slu:epsilon-p-108679
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-108679
Additional ID:
Type of IDID
DOI10.1128/mSystems.00316-20
Web of Science (WoS)000579368300031
ID Code:18692
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Dept. of Aquatic Sciences and Assessment
Deposited By: SLUpub Connector
Deposited On:18 Nov 2020 15:43
Metadata Last Modified:18 Nov 2020 15:51

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