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.
Phytoplankton are major contributors of labile dissolved organic matter to marine euphotic zone ecosystems. Viral-mediated phytoplankton lysis releases a considerable amount of bioavailable cellular contents and facilitates localized heterotrophic bacterial growth. The rapid turnover times of this labile organic matter renders it difficult to trace their transformation within natural environments. In the present study, we used a model phototroph-heterotroph coculture system to investigate the organic molecular variation during cyanophageinduced Synechococcus lysis and post-lysis periods using fluorescence spectroscopy and ultrahigh resolution mass spectrometry analyses. Approximately 80% of the Synechococcus lysates were respired to carbon dioxide within 2 days coupled to rapid regeneration of inorganic nutrients. Five fluorescent dissolved organic matter components were detected in the incubations including four humic-like and one protein-like components, and their abundances varied markedly with the succession of the viral lysis process. Viral lysis promoted the transformation of Synechococcus biomass to dissolved organic matter, and heterotrophic bacterial metabolism facilitated the transformation of organic molecules from relatively high (avg.~430 Da) to low (avg.~360 Da) molecular weight, corresponding to variation in their bioavailability. The Synechococcus-derived organic matter was highly enriched in N-containing organic molecules. Identified metabolites within the cultures primarily comprised amino acids or oligopeptides and other low-molecular-weight organic acids, carbohydrates, nucleotides, lipids, biogenic amines, and porphyrins. Among these, oligopeptides, nucleotides, and lipid compounds significantly increased with viral lysis. These results provide insight into biogeochemical cycling mediated by viral shunts in oceans, thus deepening our understanding of microbial food webs at the molecular level. Marine phytoplankton play important roles in global biogeochemical cycles and are major primary producers in euphotic oceans (Falkowski et al. 1998; Field et al. 1998; Azam and Malfatti 2007). Approximately 10% of the carbon fixed by phytoplankton is subsequently released into surrounding seawaters in the form of dissolved organic matter (DOM) via secretion, natural cellular decay, viral lysis, and protistan predation (Azam et al. 1983; Suttle 2007; Fiore et al. 2015). The labile organic matter is then directly taken up and metabolized by heterotrophic bacteria, thereby underlying the marine microbial loop (Azam et al. 1983; Kirchman 2004). Marine picocyanobacteria, including Synechococcus and Prochlorococcus, are the most numerous photosynthetic organisms on Earth and contribute to a quarter of global primary production (Field et al. 1998; Scanlan et al. 2009; Flombaum et al. 2013). Cyanophages that infect cyanobacteria are equally as abundant as their hosts, with up to~20-40% of cyanobacteria being infected and lysed every day in the ocean, thereby coupling the transformation of cyanobacterial
Aerobic anoxygenic phototrophic bacteria (AAPB) are bacteriochlorophyll a (Bchl a)-containing microbial functional population. Erythrobacter is the first genus that was identified to contain AAPB species. Here, we compared 14 Erythrobacter genomes: seven phototrophic strains and seven non- phototrophic strains. Interestingly, AAPB strains are scattered in this genus based on their phylogenetic relationships. All 14 strains could be clustered into three groups based on phylo-genomic analysis, average genomic nucleotide identity and the phylogeny of signature genes (16S rRNA and virB4 genes). The AAPB strains were distributed in three groups, and gain and loss of phototrophic genes co-occurred in the evolutionary history of the genus Erythrobacter. The organization and structure of photosynthesis gene clusters (PGCs) in seven AAPB genomes displayed high synteny of major regions except for few insertions. The 14 Erythrobacter genomes had a large range of genome sizes, from 2.72 to 3.60 M, and the sizes of the core and pan- genomes were 1231 and 8170 orthologous clusters, respectively. Integrative and conjugative elements (ICEs) were frequently identified in genomes we studied, which might play significant roles in shaping or contributing to the pan-genome of Erythrobacter. Our findings suggest the ongoing evolutionary divergence of Erythrobacter genomes and the scattered distribution characteristic of PGC.
Viral lysis and protistan grazing are thought to be the major processes leading to microbial mortality in aquatic environments and thus regulate community diversity and biogeochemical cycling characteristics. Here, we studied nutrient cycling and bacterial responses to cyanophage-mediated photoautotroph lysis and ciliate predation in a model Synechococcus-heterotroph co-culture system. Both viral lysis and Euplotes grazing facilitated the transformation of organic carbon from biomass to dissolved organic matter with convention efficiencies of 20%-26%. The accumulation of ammonium after the addition of phages and ciliates suggested the importance of recycled NH 4 + occurred in the interactions between Synechococcus growth and heterotrophic bacterial metabolism of photosynthate. The slower efficiency of P mineralization compared to N (primarily ammonium) indicated that P-containing organic matter was primarily integrated into bacterial biomass rather than being remineralized into inorganic phosphate under C-rich conditions. In the cyanophage addition treatment, both Fluviicola and Alteromonas exhibited rapid positive responses to Synechococcus lysing, while Marivita exhibited an apparent negative response. Further, the addition of Euplotes altered the incubation system from a Synechococcus-driven phycosphere to a ciliate-remodelled zoosphere that primarily constituted grazing-resistant bacteria and Euplotes symbionts. Top-down controls increased co-culture system diversity and resulted in a preference for free-living lifestyles of dominant populations, which was accompanied by the transfer of matter and energy. Our results indicate topdown control was particularly important for organic matter redistribution and inorganic nutrient regeneration between photoautotrophs and heterotrophs, and altered bacterial lifestyles. This study consequently sheds light on marine biogeochemical cycling and the interaction networks within these dynamic ecosystems.
Aerobic anoxygenic photoheterotrophic bacteria (AAPB) represent a bacteriochlorophyll a-containing functional group. Substantial evidence indicates that highly conserved photosynthetic gene clusters (PGCs) of AAPB can be transferred between species, genera, and even phyla. Furthermore, analysis of recently discovered PGCs carried by extrachromosomal replicons (exPGCs) suggests that extrachromosomal replicons (ECRs) play an important role in the transfer of PGCs. In this study, 13 Roseobacter clade genomes from seven genera that harbored exPGCs were used to analyze the characteristics and evolution of PGCs. The identification of plasmid-like and chromid-like ECRs among PGC-containing ECRs revealed two different functions: the spread of PGCs among strains and the maintenance of PGCs within genomes. Phylogenetic analyses indicated two independent origins of exPGCs, corresponding to PufC-containing and PufX-containing puf operons. Furthermore, the two different types of operons were observed within different strains of the same Tateyamaria and Jannaschia genera. The PufC-containing and PufX-containing operons were also differentially carried by chromosomes and ECRs in the strains, respectively, which provided clear evidence for ECR-mediated PGC transfer. Multiple recombination events of exPGCs were also observed, wherein the majority of exPGCs were inserted by replication modules at the same genomic positions. However, the exPGCs of the Jannaschia strains comprised superoperons without evidence of insertion and therefore likely represent an initial evolutionary stage where the PGC was translocated from chromosomes to ECRs without further combinations. Finally, a scenario of PGC gain and loss is proposed that specifically focuses on ECR-mediated exPGC transfer to explain the evolution and patchy distribution of AAPB within the Roseobacter clade. IMPORTANCE The evolution of photosynthesis was a significant event during the diversification of biological life. Aerobic anoxygenic photoheterotrophic bacteria (AAPB) share physiological characteristics with chemoheterotrophs and represent an important group associated with bacteriochlorophyll-dependent phototrophy in the environment. Here, characterization and evolutionary analyses were conducted for 13 bacterial strains that contained photosynthetic gene clusters (PGCs) carried by extrachromosomal replicons (ECRs) to shed light on the evolution of chlorophototrophy in bacteria. This report advances our understanding of the importance of ECRs in the transfer of PGCs within marine photoheterotrophic bacteria.
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