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.
Highlights
Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments
Marine bacteria take up labile dissolved organic carbon (DOC) that is released by phytoplankton into surrounding waters, and they transform a fraction of this DOC into recalcitrant forms via a series of metabolic processes collectively referred to as the microbial carbon pump [6]
Synechococcus strain YX04-3 was isolated from the South China Sea using PRO2 liquid medium and purified after ϳ5 to 7 rounds of dilution until a single Synechococcus internal transcribed spacer (ITS) sequence was obtained [25]
Summary
Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. Isolated marine unicellular cyanobacterial cultures, including those of Synechococcus and Prochlorococcus, typically contain coexisting heterotrophic bacterial partners [17, 18] Such associations between Synechococcus and heterotrophic bacteria have been observed in natural environments [19]. The interactions between picocyanobacteria and single heterotrophic bacterial strains (e.g., Synechococcus-Ruegeria pomeroyi DSS-3, SynechococcusShewanella, Synechococcus-Vibrio, and Prochlorococcus-Alteromonas) have been thoroughly investigated, yielding evidence for synergistic relationships among the two partners in coculture systems [8, 20,21,22,23,24]. In situ interaction networks between photoautotrophs and heterotrophs are two-member systems but instead comprise diverse heterotrophic bacterial assemblies associated with a single photoautotrophic strain These myriad relationships are synergistic in nature and competitive and antagonistic
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