Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture

ABSTRACT Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. Here, bacterial community composition, lifestyle preference, and genomic- and proteomic-level metabolic characteristics were investigated for...

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Autores principales:	Qiang Zheng, Yu Wang, Jiayao Lu, Wenxin Lin, Feng Chen, Nianzhi Jiao
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Synechococcus culture interactions high-molecular-weight DOM low-molecular-weight DOM metagenome metaproteome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6eaef949438a46cab6234ef56c47124b
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spelling	oai:doaj.org-article:6eaef949438a46cab6234ef56c47124b2021-11-15T15:56:58ZMetagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture10.1128/mBio.03261-192150-7511https://doaj.org/article/6eaef949438a46cab6234ef56c47124b2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03261-19https://doaj.org/toc/2150-7511ABSTRACT Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. Here, bacterial community composition, lifestyle preference, and genomic- and proteomic-level metabolic characteristics were investigated for an open ocean Synechococcus ecotype and its associated heterotrophs over 91 days of cocultivation. The associated heterotrophic bacterial assembly mostly constituted five classes, including Flavobacteria, Bacteroidetes, Phycisphaerae, Gammaproteobacteria, and Alphaproteobacteria. The seven most abundant taxa/genera comprised >90% of the total heterotrophic bacterial community, and five of these displayed distinct lifestyle preferences (free-living or attached) and responses to Synechococcus growth phases. Six high-quality genomes, including Synechococcus and the five dominant heterotrophic bacteria, were reconstructed. The only primary producer of the coculture system, Synechococcus, displayed metabolic processes primarily involved in inorganic nutrient uptake, photosynthesis, and organic matter biosynthesis and release. Two of the flavobacterial populations, Muricauda and Winogradskyella, and an SM1A02 population, displayed preferences for initial degradation of complex compounds and biopolymers, as evinced by high abundances of TonB-dependent transporters (TBDTs), glycoside hydrolase, and peptidase proteins. Polysaccharide utilization loci present in the flavobacterial genomes influence their lifestyle preferences and close associations with phytoplankton. In contrast, the alphaproteobacterium Oricola sp. population mainly utilized low-molecular-weight dissolved organic carbon (DOC) through ATP-binding cassette (ABC), tripartite ATP-independent periplasmic (TRAP), and tripartite tricarboxylate transporter (TTT) transport systems. The heterotrophic bacterial populations exhibited complementary mechanisms for degrading Synechococcus-derived organic matter and driving nutrient cycling. In addition to nutrient exchange, removal of reactive oxygen species and vitamin trafficking might also contribute to the maintenance of the Synechococcus-heterotroph coculture system and the interactions shaping the system. IMPORTANCE The high complexity of in situ ecosystems renders it difficult to study marine microbial photoautotroph-heterotroph interactions. Two-member coculture systems of picocyanobacteria and single heterotrophic bacterial strains have been thoroughly investigated. However, in situ interactions comprise far more diverse heterotrophic bacterial associations with single photoautotrophic organisms. In the present study, combined metagenomic and metaproteomic data supplied the metabolic potentials and activities of uncultured dominant bacterial populations in the coculture system. The results of this study shed light on the nature of interactions between photoautotrophs and heterotrophs, improving our understanding of the complexity of in situ environments.Qiang ZhengYu WangJiayao LuWenxin LinFeng ChenNianzhi JiaoAmerican Society for MicrobiologyarticleSynechococcus cultureinteractionshigh-molecular-weight DOMlow-molecular-weight DOMmetagenomemetaproteomeMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Synechococcus culture interactions high-molecular-weight DOM low-molecular-weight DOM metagenome metaproteome Microbiology QR1-502
spellingShingle	Synechococcus culture interactions high-molecular-weight DOM low-molecular-weight DOM metagenome metaproteome Microbiology QR1-502 Qiang Zheng Yu Wang Jiayao Lu Wenxin Lin Feng Chen Nianzhi Jiao Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture
description	ABSTRACT Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. Here, bacterial community composition, lifestyle preference, and genomic- and proteomic-level metabolic characteristics were investigated for an open ocean Synechococcus ecotype and its associated heterotrophs over 91 days of cocultivation. The associated heterotrophic bacterial assembly mostly constituted five classes, including Flavobacteria, Bacteroidetes, Phycisphaerae, Gammaproteobacteria, and Alphaproteobacteria. The seven most abundant taxa/genera comprised >90% of the total heterotrophic bacterial community, and five of these displayed distinct lifestyle preferences (free-living or attached) and responses to Synechococcus growth phases. Six high-quality genomes, including Synechococcus and the five dominant heterotrophic bacteria, were reconstructed. The only primary producer of the coculture system, Synechococcus, displayed metabolic processes primarily involved in inorganic nutrient uptake, photosynthesis, and organic matter biosynthesis and release. Two of the flavobacterial populations, Muricauda and Winogradskyella, and an SM1A02 population, displayed preferences for initial degradation of complex compounds and biopolymers, as evinced by high abundances of TonB-dependent transporters (TBDTs), glycoside hydrolase, and peptidase proteins. Polysaccharide utilization loci present in the flavobacterial genomes influence their lifestyle preferences and close associations with phytoplankton. In contrast, the alphaproteobacterium Oricola sp. population mainly utilized low-molecular-weight dissolved organic carbon (DOC) through ATP-binding cassette (ABC), tripartite ATP-independent periplasmic (TRAP), and tripartite tricarboxylate transporter (TTT) transport systems. The heterotrophic bacterial populations exhibited complementary mechanisms for degrading Synechococcus-derived organic matter and driving nutrient cycling. In addition to nutrient exchange, removal of reactive oxygen species and vitamin trafficking might also contribute to the maintenance of the Synechococcus-heterotroph coculture system and the interactions shaping the system. IMPORTANCE The high complexity of in situ ecosystems renders it difficult to study marine microbial photoautotroph-heterotroph interactions. Two-member coculture systems of picocyanobacteria and single heterotrophic bacterial strains have been thoroughly investigated. However, in situ interactions comprise far more diverse heterotrophic bacterial associations with single photoautotrophic organisms. In the present study, combined metagenomic and metaproteomic data supplied the metabolic potentials and activities of uncultured dominant bacterial populations in the coculture system. The results of this study shed light on the nature of interactions between photoautotrophs and heterotrophs, improving our understanding of the complexity of in situ environments.
format	article
author	Qiang Zheng Yu Wang Jiayao Lu Wenxin Lin Feng Chen Nianzhi Jiao
author_facet	Qiang Zheng Yu Wang Jiayao Lu Wenxin Lin Feng Chen Nianzhi Jiao
author_sort	Qiang Zheng
title	Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture
title_short	Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture
title_full	Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture
title_fullStr	Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture
title_full_unstemmed	Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture
title_sort	metagenomic and metaproteomic insights into photoautotrophic and heterotrophic interactions in a <italic toggle="yes">synechococcus</italic> culture
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/6eaef949438a46cab6234ef56c47124b
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Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <italic toggle="yes">Synechococcus</italic> Culture

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