Marine phytoplankton blooms are annual spring events that sustain active and diverse bloom-associated bacterial populations. Blooms vary considerably in terms of eukaryotic species composition and environmental conditions, but a limited number of heterotrophic bacterial lineages - primarily members of the Flavobacteriia, Alphaproteobacteria and Gammaproteobacteria - dominate these communities. In this Review, we discuss the central role that these bacteria have in transforming phytoplankton-derived organic matter and thus in biogeochemical nutrient cycling. On the basis of selected field and laboratory-based studies of flavobacteria and roseobacters, distinct metabolic strategies are emerging for these archetypal phytoplankton-associated taxa, which provide insights into the underlying mechanisms that dictate their behaviours during blooms.
3Despite the overwhelming bacterial diversity present in the world's oceans, the majority of recognized marine bacteria fall into as few as nine major clades (36), many of which have yet to be cultivated in the laboratory. Molecular-based approaches targeting 16S rRNA genes demonstrate that the Roseobacter clade is one of these major marine groups, typically comprising upwards of 20% of coastal and 15% of mixed-layer ocean bacterioplankton communities (see, e.g., references 36, 37, 42, 98, and 109). Roseobacters are well represented across diverse marine habitats, from coastal to open oceans and from sea ice to sea floor (see, e.g., references 16, 28, 37, 42, 52, and 98). Members have been found to be free living, particle associated, or in commensal relationships with marine phytoplankton, invertebrates, and vertebrates (see, e.g., references 4, 6, 7, 44, 49, 115, and 119). Furthermore, representatives of the clade stand out as representing one of the most readily cultivated of the major marine lineages (36). These isolated representatives are serving as the foundation for an improved understanding of marine bacterial ecology and physiology. DESCRIPTION OF THE GROUPThe Roseobacter clade falls within the ␣-3 subclass of the class Proteobacteria, with members sharing Ͼ89% identity of the 16S rRNA gene. The first strain descriptions appeared in 1991, about the time that 16S rRNA-based approaches for cataloging microbial diversity were revealing the immensity of prokaryotic diversity in the world's oceans. Interest in the clade has risen steadily since the initial discovery of these strains; at present the clade contains 36 described species, representing 17 genera, and literally hundreds of uncharacterized isolates and clone sequences. The first described members were Roseobacter litoralis and Roseobacter denitrificans, both pinkpigmented bacteriochlorophyll a-producing strains isolated from marine algae (99). Subsequent cultivation of clade members, however, revealed that many strains are neither pink nor bacteriochlorophyll a producers (see, e.g., references 20, 41, 43, and 61). With the exceptions of the described strains of the genus Ketogulonicigenium (113) and several clones from a South African gold mine (GenBank accession numbers AF546906, -13, -17, -22 to -24, and -26), the Roseobacter clade is exclusively marine or hypersaline, with characterized isolates demonstrating either a salt requirement or tolerance (see, e.g., references 60 and 62 ABUNDANCE AND DISTRIBUTION IN MARINE ENVIRONMENTSBased on culture collections, 16S rRNA clone libraries, and single-cell analyses, roseobacters have been identified in most marine environments sampled. The group is prevalent in 16S rRNA gene inventories of seawater (Table 1) and marine sediments (Table 2) and is noticeably absent from analogous inventories of freshwater and terrestrial soil environments. Fluorescent in situ hybridization (FISH) studies quantifying Roseobacter populations in coastal waters of the southeastern United States and the North Sea indicate ...
Flux of dimethylsulfide (DMS) from ocean surface waters is the predominant natural source of sulfur to the atmosphere and influences climate by aerosol formation. Marine bacterioplankton regulate sulfur flux by converting the precursor dimethylsulfoniopropionate (DMSP) either to DMS or to sulfur compounds that are not climatically active. Through the discovery of a glycine cleavage T-family protein with DMSP methyltransferase activity, marine bacterioplankton in the Roseobacter and SAR11 taxa were identified as primary mediators of DMSP demethylation to methylmercaptopropionate. One-third of surface ocean bacteria harbor a DMSP demethylase homolog and thereby route a substantial fraction of global marine primary production away from DMS formation and into the marine microbial food web.
Bacterioplankton of the marine Roseobacter clade have genomes that reflect a dynamic environment and diverse interactions with marine plankton. Comparative genome sequence analysis of three cultured representatives suggests that cellular requirements for nitrogen are largely provided by regenerated ammonium and organic compounds (polyamines, allophanate, and urea), while typical sources of carbon include amino acids, glyoxylate, and aromatic metabolites. An unexpectedly large number of genes are predicted to encode proteins involved in the production, degradation, and efflux of toxins and metabolites. A mechanism likely involved in cell-to-cell DNA or protein transfer was also discovered: vir-related genes encoding a type IV secretion system typical of bacterial pathogens. These suggest a potential for interacting with neighboring cells and impacting the routing of organic matter into the microbial loop. Genes shared among the three roseobacters and also common in nine draft Roseobacter genomes include those for carbon monoxide oxidation, dimethylsulfoniopropionate demethylation, and aromatic compound degradation. Genes shared with other cultured marine bacteria include those for utilizing sodium gradients, transport and metabolism of sulfate, and osmoregulation.In surface waters of the open ocean, 1 in 10 bacterial cells is a member of the Roseobacter group (17). In coastal waters, the number of Roseobacter cells increases to 1 in 5 (11, 19). Despite their obvious ecological success, however, roseobacters do not fit the stereotype of a small, metabolically conservative, "oligotrophic" bacterium (8, 18). Instead, they are large (0.08 m 3 ) (38), easily cultured (19), and respond readily to increased substrate availability (7). Analysis of the first Roseobacter genome sequence, that of Silicibacter pomeroyi, revealed a fairly large genome (4.5 Mb) housing abundant and diverse transporters, complex regulatory systems, and multiple pathways for acquiring carbon and energy in seawater. Roseobacters thus appear to be quite versatile from metabolic and ecological standpoints (43), with an assortment of strategies for obtaining carbon and nutrients and, directly or indirectly, affecting the biogeochemical status of seawater.The availability of two additional closed genome sequences of cultured roseobacters provides the opportunity for an ecologically based analysis of the genetic capabilities of this bacterial taxon. The three organisms are assumed to have different niches in the surface ocean based on the conditions of their isolation: S. pomeroyi is a free-living heterotrophic bacterioplankter obtained from coastal seawater (43), congener Silicibacter sp. strain TM1040 (96% 16S rRNA sequence identity to S. pomeroyi [ Fig. 1]) is an associate of the marine dinoflagellate Pfiesteria piscicida (1, 40), and Jannaschia sp. strain CCS1 (with 94% 16S rRNA sequence identity to the two Silicibacter species) represents a recently discovered class of marine aerobic bacteriochlorophyll a-based phototrophs (4). Our comparative an...
In marine environments, virus-mediated lysis of host cells leads to the release of cellular carbon and nutrients and is hypothesized to be a major driver of carbon recycling on a global scale. However, efforts to characterize the effects of viruses on nutrient cycles have overlooked the geochemical potential of the virus particles themselves, particularly with respect to their phosphorus content. In this Analysis article, we use a biophysical scaling model of intact virus particles that has been validated using sequence and structural information to quantify differences in the elemental stoichiometry of marine viruses compared with their microbial hosts. By extrapolating particle-scale estimates to the ecosystem scale, we propose that, under certain circumstances, marine virus populations could make an important contribution to the reservoir and cycling of oceanic phosphorus.
Marine viruses are critical drivers of ocean biogeochemistry and their abundances vary spatiotemporally in the global oceans, with upper estimates exceeding 10 8 per ml. Over many years, a consensus has emerged that virus abundances are typically 10-fold higher than prokaryote abundances. The use of a fixed-ratio suggests that the relationship between virus and prokaryote abundances is both predictable and linear. However, the true explanatory power of a linear relationship and its robustness across diverse ocean environments is unclear. Here, we compile 5671 prokaryote and virus abundance estimates from 25 distinct marine surveys to characterize the relationship between virus and prokaryote abundances. We find that the median virus-to-prokaryote ratio (VPR) is 10:1 and 16:1 in the near-and sub-surface oceans, respectively. Nonetheless, we observe substantial variation in the VPR and find either no or limited explanatory power using fixed-ratio models. Instead, virus abundances are better described as nonlinear, power-law functions of prokaryote abundances -particularly when considering relationships within distinct marine surveys. Estimated power-laws have scaling exponents that are typically less than 1, signifying that the VPR decreases with prokaryote density, rather than remaining fixed. The emergence of power-law scaling presents a challenge for mechanistic models seeking to understand the ecological causes and consequences of marine virusmicrobe interactions. Such power-law scaling also implies that efforts to average viral effects on microbial mortality and biogeochemical cycles using "representative" abundances or abundanceratios need to be refined if they are to be utilized to make quantitative predictions at regional or global ocean scales.
Dissolved organic matter (DOM) in the oceans is one of the largest pools of reduced carbon on Earth, comparable in size to the atmospheric CO 2 reservoir. A vast number of compounds are present in DOM, and they play important roles in all major element cycles, contribute to the storage of atmospheric CO 2 in the ocean, support marine ecosystems, and facilitate interactions between organisms. At the heart of the DOM cycle lie molecular-level relationships between the individual compounds in DOM and the members of the ocean microbiome that produce and consume them. In the past, these connections have eluded clear definition because of the sheer numerical complexity of both DOM molecules and microorganisms. Emerging tools in analytical chemistry, microbiology, and informatics are breaking down the barriers to a fuller appreciation of these connections. Here we highlight questions being addressed using recent methodological and technological developments in those fields and consider how these advances are transforming our understanding of some of the most important reactions of the marine carbon cycle.dissolved organic matter | marine microbes | cyberinfrastructure
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