Dataset Information

Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a Synechococcus 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 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.

SUBMITTER: Zheng Q

PROVIDER: S-EPMC7029141 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a Synechococcus Culture.

Zheng Qiang Q Wang Yu Y Lu Jiayao J Lin Wenxin W Chen Feng F Jiao Nianzhi N

mBio 20200218 1

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 Flavobact ...[more]

PMID: 32071270

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Project description:Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. However, the high complexity of in situ ecosystems renders it difficult to study these interactions. Two-member co-culture 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. 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 co-cultivation. 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 from the co-culture system were reconstructed inclusive of Synechococcus and the five dominant heterotrophic bacterial populations. The only primary producer of the co-culture 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 TBDT, glycoside hydrolase, and peptidases proteins. In contrast, the alphaproteobacterium Oricola sp. population mainly utilized low molecular weight DOM, including Flavobacteria metabolism byproducts, through ABC, TRAP, and TTT transport systems. Polysaccharide-utilization loci present in the flavobacterial genomes encoded similar trans-membrane protein complexes as Sus/cellulosome and may influence their lifestyle preferences and close associations with phytoplankton. 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 also contributed to the maintenance of the Synechococcus / heterotroph co-culture system and the interactions shaping the system.

Project description:Viruses are infectious and abundant in the marine environment. Viral lysis of host cells releases organic matter and nutrients that affect the surrounding microbial community. Synechococcus are important primary producers in the ocean and they are subject to frequent viral infection. In the laboratory, Synechococcus cultures are often associated with bacteria and such a co-existence relationship appears to be important to the growth and stability of Synechococcus. However, we know little about how viral lysis of Synechococcus affects the co-existing bacteria in the culture. This study investigated the influence of viral infection of Synechococcus on co-occurring bacterial community in the culture. We analyzed the community composition, diversity, predicted functions of the bacterial community, and its correlations with fluorescent dissolved organic matter (FDOM) components and nutrients after introducing a cyanophage to the Synechococcus culture. Cyanophage infection altered the bacterial community structure and increased the bacterial diversity and richness. Increased bacterial groups such as Bacteroidetes and Alphaproteobacteria and decreased bacterial groups such as Gammaproteobacteria were observed. Moreover, cyanophage infection reduced bacterial interactions but enhanced correlations between the dominant bacterial taxa and nutrients. Unique FDOM components were observed in the cyanophage-added culture. Fluorescence intensities of FDOM components varied across the cyanophage-infection process. Decreased nitrate and increased ammonium and phosphate in the cyanophage-added culture coupled with the viral progeny production and increased substance transport and metabolism potentials of the bacterial community. Furthermore, increased potentials in methane metabolism and aromatic compound degradation of the bacterial community were observed in the cyanophage-added culture, suggesting that cyanophage infections contribute to the production of methane-related compounds and refractory organic matter in a microcosm like environment. This study has the potential to deepen our understanding of the impact of viral lysis of cyanobacteria on microbial community in the surrounding water.

Project description:Interactions between photoautotrophic and heterotrophic microorganisms are central to the marine microbial ecosystem. Lab cultures of one of the dominant marine photoautotrophs, Synechococcus, have historically been difficult to render axenic, presumably because these bacteria depend upon other organisms to grow under these conditions. These tight associations between Synechococcus and heterotrophic bacteria represent a good relevant system to study interspecies interactions. Ten individual Synechococcus strains, isolated from eutrophic and oligotrophic waters, were chosen for investigation. Four to six dominant associated heterotrophic bacteria were detected in the liquid cultures of each Synechococcus isolate, comprising members of the Cytophaga-Flavobacteria-Bacteroides (CFB) group (mainly from Flavobacteriales and Cytophagales), Alphaproteobacteria (mainly from the Roseobacter clade), Gammaproteobacteria (mainly from the Alteromonadales and Pseudomonadales), and Actinobacteria The presence of the CFB group, Gammaproteobacteria, and Actinobacteria showed clear geographic patterns related to the isolation environments of the Synechococcus bacteria. An investigation of the population dynamics within a growing culture (XM-24) of one of the isolates, including an evaluation of the proportions of cells that were free-living versus aggregated/attached, revealed interesting patterns for different bacterial groups. In Synechococcus sp. strain XM-24 culture, flavobacteria, which was the most abundant group throughout the culture period, tended to be aggregated or attached to the Synechococcus cells, whereas the actinobacteria demonstrated a free-living lifestyle, and roseobacters displayed different patterns depending on the culture growth phase. Factors contributing to these succession patterns for the heterotrophs likely include interactions among the culture community members, their relative abilities to utilize different compounds produced by Synechococcus cells and changes in the compounds released as culture growth proceeds, and their responses to other changes in the environmental conditions throughout the culture period.IMPORTANCE Marine microbes exist within an interactive ecological network, and studying their interactions is an important part of understanding their roles in global biogeochemical cycling and the determinants of microbial diversity. In this study, the dynamic relationships between Synechococcus spp. and their associated heterotrophic bacteria were investigated. Synechococcus-associated heterotrophic bacteria had similar geographic distribution patterns as their "host" and displayed different lifestyles (free-living versus attached/aggregated) according to the Synechococcus culture growth phases. Combined organic carbon composition and bacterial lifestyle data indicated a potential for succession in carbon utilization patterns by the dominant associated heterotrophic bacteria. Comprehending the interactions between photoautotrophs and heterotrophs and the patterns of organic carbon excretion and utilization is critical to understanding their roles in oceanic biogeochemical cycling.

Dataset Information

Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a Synechococcus Culture.

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Metagenomic and Metaproteomic Insights into Photoautotrophic and Heterotrophic Interactions in a <i>Synechococcus</i> Culture.

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