Marine microbes are major drivers of all elemental cycles. The processing of organic carbon by heterotrophic prokaryotes is tightly coupled to the availability of the trace element iron in large ...regions of the Southern Ocean. However, the functional diversity in iron and carbon metabolism within diverse communities remains a major unresolved issue. Using novel Southern Ocean meta-omics resources including 133 metagenome-assembled genomes (MAGs), we show a mosaic of taxonomy-specific ecological strategies in naturally iron-fertilized and high nutrient low chlorophyll (HNLC) waters. Taxonomic profiling revealed apparent community shifts across contrasting nutrient regimes. Community-level and genome-resolved metatranscriptomics evidenced a moderate association between taxonomic affiliations and iron and carbon-related functional roles. Diverse ecological strategies emerged when considering the central metabolic pathways of individual MAGs. Closely related lineages appear to adapt to distinct ecological niches, based on their distribution and gene regulation patterns. Our in-depth observations emphasize the complex interplay between the genetic repertoire of individual taxa and their environment and how this shapes prokaryotic responses to iron and organic carbon availability in the Southern Ocean.
Deciphering ocean carbon in a changing world Moran, Mary Ann; Elizabeth B. Kujawinski; Aron Stubbins ...
Proceedings of the National Academy of Sciences - PNAS,
03/2016, Letnik:
113, Številka:
12
Journal Article
Recenzirano
Odprti dostop
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 â 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 â 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.
Summary
The interplay among microorganisms profoundly impacts biogeochemical cycles in the ocean. Culture‐based work has illustrated the diversity of diatom–prokaryote interactions, but the question ...of whether these associations can affect the spatial distribution of microbial communities is open. Here, we investigated the relationship between assemblages of diatoms and of heterotrophic prokaryotes in surface waters of the Indian sector of the Southern Ocean in early spring. The community composition of diatoms and that of total and active prokaryotes were different among the major ocean zones investigated. We found significant relationships between compositional changes of diatoms and of prokaryotes. In contrast, spatial changes in the prokaryotic community composition were not related to geographic distance and to environmental parameters when the effect of diatoms was accounted for. Diatoms explained 30% of the variance in both the total and the active prokaryotic community composition in early spring in the Southern Ocean. Using co‐occurrence analyses, we identified a large number of highly significant correlations between abundant diatom species and prokaryotic taxa. Our results show that key diatom species of the Southern Ocean are each associated with a distinct prokaryotic community, suggesting that diatom assemblages contribute to shaping the habitat type for heterotrophic prokaryotes.
The photo- and bioreactive components of dissolved organic matter (DOM) from three different environments were determined during long-term decomposition experiments. Terrigenous DOM was collected ...from a black-water system, plankton DOM was harvested from phytoplankton cultures, and lake water served as a DOM source with both terrigenous and plankton components. Photomineralization accounted for the removal of 46 and 7% of terrigenous and lake-dissolved organic carbon (DOC), respectively, while no loss in DOC was observed when plankton DOM was exposed to irradiation. Biomineralization accounted for the removal of 27% each of terrigenous and lake DOC and 74% of plankton DOC. Phototransformations of terrigenous and lake DOM resulted in 7% and 2% increases in biodegradable DOC, respectively, while no increase in biodegradable DOC was observed for irradiated plankton DOM. In two different experimental approaches, terrigenous DOM was exposed to sequential and alternating bio- and photodegradation, respectively, to determine the fractions of DOC that were bioreactive and photoreactive. About 15% of terrigenous DOC was susceptible to both biomineralization and photomineralization. These results demonstrate that biological and photochemical processes compete in the mineralization of DOC. Photomineralization of bioreactive DOC is likely an important factor determining the net effect of irradiation on the bioreactivity of DOM.
The ecology of the SAR11 clade, the most abundant bacterial group in the ocean, has been intensively studied in temperate and tropical regions, but its distribution remains largely unexplored in the ...Southern Ocean. Through amplicon sequencing of the 16S rRNA gene, we assessed the contribution of the SAR11 clade to bacterial community composition in the naturally iron fertilized region off Kerguelen Island. We investigated the upper 300 m at seven sites located in early spring phytoplankton blooms and at one high‐nutrient low‐chlorophyll site. Despite pronounced vertical patterns of the bacterioplankton assemblages, the SAR11 clade had high relative abundances at all depths and sites, averaging 40% (±15%) of the total community relative abundance. Micro‐autoradiography combined with CARD‐FISH further revealed that the clade had an overall stable contribution (45%–60% in surface waters) to bacterial biomass production (determined by 3H‐leucine incorporation) during different early bloom stages. The spatio‐temporal partitioning of some of the SAR11 subclades suggests a niche specificity and periodic selection of different subclades in response to the fluctuating extreme conditions of the Southern Ocean. These observations improve our understanding of the ecology of the SAR11 clade and its implications in biogeochemical cycles in the rapidly changing Southern Ocean.
Summary
Marine heterotrophic prokaryotes (HP) play a key role in organic matter processing in the ocean; however, the view of HP as dissolved organic matter (DOM) sources remains underexplored. In ...this study, we quantified and optically characterized the DOM produced by two single marine bacterial strains. We then tested the availability of these DOM sources to in situ Mediterranean Sea HP communities. Two bacterial strains were used: Photobacterium angustum (a copiotrophic gammaproteobacterium) and Sphingopyxis alaskensis (an oligotrophic alphaproteobacterium). When cultivated on glucose as the sole carbon source, the two strains released from 7% to 23% of initial glucose as bacterial derived DOM (B‐DOM), the quality of which (as enrichment in humic or protein‐like substances) differed between strains. B‐DOM induced significant growth and carbon consumption of natural HP communities, suggesting that it was partly labile. However, B‐DOM consistently promoted lower prokaryotic growth efficiencies than in situ DOM. In addition, B‐DOM changed HP exoenzymatic activities, enhancing aminopeptidase activity when degrading P. angustum DOM, and alkaline phosphatase activity when using S. alaskensis DOM, and promoted differences in HP diversity and composition. DOM produced by HP affects in situ prokaryotic metabolism and diversity, thus changing the pathways for DOM cycling (e.g. respiration over biomass production) in the ocean.
Abstract
Background
Heterotrophic microbes in the Southern Ocean are challenged by the double constraint of low concentrations of organic carbon (C) and iron (Fe). These essential elements are ...tightly coupled in cellular processes; however, the prokaryotic requirements of C and Fe under varying environmental settings remain poorly studied. Here, we used a combination of metatranscriptomics and metaproteomics to identify prokaryotic membrane transporters for organic substrates and Fe in naturally iron-fertilized and high-nutrient, low-chlorophyll waters of the Southern Ocean during spring and late summer.
Results
Pronounced differences in membrane transporter profiles between seasons were observed at both sites, both at the transcript and protein level. When specific compound classes were considered, the two approaches revealed different patterns. At the transcript level, seasonal patterns were only observed for subsets of genes belonging to each transporter category. At the protein level, membrane transporters of organic compounds were relatively more abundant in spring as compared to summer, while the opposite pattern was observed for Fe transporters. These observations suggest an enhanced requirement for organic C in early spring and for Fe in late summer. Mapping transcripts and proteins to 50 metagenomic-assembled genomes revealed distinct taxon-specific seasonal differences pointing to potentially opportunistic clades, such as Pseudomonadales and
Nitrincolaceae,
and groups with a more restricted repertoire of expressed transporters, such as Alphaproteobacteria and
Flavobacteriaceae
.
Conclusion
The combined investigations of C and Fe membrane transporters suggest seasonal changes in the microbial requirements of these elements under different productivity regimes. The taxon-specific acquisition strategies of different forms of C and Fe illustrate how diverse microbes could shape transcript and protein expression profiles at the community level at different seasons. Our results on the C- and Fe-related metabolic capabilities of microbial taxa provide new insights into their potential role in the cycling of C and Fe under varying nutrient regimes in the Southern Ocean.
A seven-year oceanographic time series in NW Mediterranean surface waters was combined with pyrosequencing of ribosomal RNA (16S rRNA) and ribosomal RNA gene copies (16S rDNA) to examine the ...environmental controls on SAR11 ecotype dynamics and potential activity. SAR11 diversity exhibited pronounced seasonal cycles remarkably similar to total bacterial diversity. The timing of diversity maxima was similar across narrow and broad phylogenetic clades and strongly associated with deep winter mixing. Diversity minima were associated with periods of stratification that were low in nutrients and phytoplankton biomass and characterised by intense phosphate limitation (turnover time<5 h). We propose a conceptual framework in which physical mixing of the water column periodically resets SAR11 communities to a high diversity state and the seasonal evolution of phosphate limitation competitively excludes deeper-dwelling ecotypes to promote low diversity states dominated (>80%) by SAR11 Ia. A partial least squares (PLS) regression model was developed that could reliably predict sequence abundances of SAR11 ecotypes (Q(2)=0.70) from measured environmental variables, of which mixed layer depth was quantitatively the most important. Comparison of clade-level SAR11 rRNA:rDNA signals with leucine incorporation enabled us to partially validate the use of these ratios as an in-situ activity measure. However, temporal trends in the activity of SAR11 ecotypes and their relationship to environmental variables were unclear. The strong and predictable temporal patterns observed in SAR11 sequence abundance was not linked to metabolic activity of different ecotypes at the phylogenetic and temporal resolution of our study.
The availability of iron limits primary productivity and the associated uptake of carbon over large areas of the ocean. Iron thus plays an important role in the carbon cycle, and changes in its ...supply to the surface ocean may have had a significant effect on atmospheric carbon dioxide concentrations over glacial-interglacial cycles. To date, the role of iron in carbon cycling has largely been assessed using short-term iron-addition experiments. It is difficult, however, to reliably assess the magnitude of carbon export to the ocean interior using such methods, and the short observational periods preclude extrapolation of the results to longer timescales. Here we report observations of a phytoplankton bloom induced by natural iron fertilization--an approach that offers the opportunity to overcome some of the limitations of short-term experiments. We found that a large phytoplankton bloom over the Kerguelen plateau in the Southern Ocean was sustained by the supply of iron and major nutrients to surface waters from iron-rich deep water below. The efficiency of fertilization, defined as the ratio of the carbon export to the amount of iron supplied, was at least ten times higher than previous estimates from short-term blooms induced by iron-addition experiments. This result sheds new light on the effect of long-term fertilization by iron and macronutrients on carbon sequestration, suggesting that changes in iron supply from below--as invoked in some palaeoclimatic and future climate change scenarios--may have a more significant effect on atmospheric carbon dioxide concentrations than previously thought.
One of the first comparisons of a natural iron fertilized bloom with a high-nutrient low-chlorophyll (HNLC) site was undertaken during the Kerguelen ocean and plateau compared study (KEOPS) cruise. ...To understand better the bacteria-phytoplankton relationship in the context of natural iron fertilization, bacterial diversity and activity was investigated in the bloom and in the adjacent HNLC region by 16S rDNA clone libraries and by single strand conformation polymorphism (SSCP) analysis. Both libraries were dominated by Alphaproteobacteria, Gammaproteobacteria and the Cytophaga-Flavobacteria-Bacteroides group. Cluster analysis at 99% sequence similarity yielded several microdiverse clusters and revealed striking differences between the two libraries. In the bloom, the dominant operational taxonomic units (OTUs) were the Roseobacter NAC11-7 cluster, SAR92 and a Cytophaga-Flavobacteria-Bacteroides cluster related to the agg58 group, whereas in the HNLC region, SAR11, Roseobacter RCA and Polaribacter dominated. SSCP analysis of 16S rDNA and 16S rRNA revealed contrasting dynamics of three different Roseobacter OTUs. Roseobacter NAC11-7 and NAC11-6 had higher relative abundances and activities in the bloom compared with the HNLC site and NAC11-6 was only detected at the decline of the bloom concomitant with a shift in phytoplankton composi tion. In contrast, Roseobacter RCA was relatively abundant and active both inside and outside of the bloom. These results suggest that the different OTUs within the Roseobacter group represent functional groups that each play an important role in the cycling of carbon.
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