The genomic potential of photosynthesis in piconanoplankton is functionally redundant but taxonomically structured at a global scale.

Carbon fixation is a key metabolic function shaping marine life, but the underlying taxonomic and functional diversity involved is only partially understood. Using metagenomic resources targeted at marine piconanoplankton, we provide a reproducible machine learning framework to derive the potential biogeography of genomic functions through the multi-output regression of gene read counts on environmental climatologies. Leveraging the Marine Atlas of Tara Oceans Unigenes, we investigate the genomic potential of primary production in the global ocean. The latter is performed by ribulose-1,5-bisphosphate carboxylase/oxygenase (RUBISCO) and is often associated with carbon concentration mechanisms in piconanoplankton, major marine unicellular photosynthetic organisms. We show that the genomic potential supporting C4 enzymes and RUBISCO exhibits strong functional redundancy and important affinity toward tropical oligotrophic waters. This redundancy is taxonomically structured by the dominance of Mamiellophyceae and Prymnesiophyceae in mid and high latitudes. These findings enhance our understanding of the relationship between functional and taxonomic diversity of microorganisms and environmental drivers of key biogeochemical cycles.

Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean.

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. Video Abstract.

Fungal Diversity and Community Composition across Ecosystems.

Fungi have shaped the biosphere since the development of life on Earth. Despite fungi being present in all environments, most of the available fungal research has focused on soils. As a result, the role and composition of fungal communities in aquatic (marine and freshwater) environments remain largely unexplored. The use of different primers to characterise fungal communities has additionally complicated intercomparisons among studies. Consequently, we lack a basic global assessment of fungal diversity across major ecosystems. Here, we took advantage of a recently published 18S rRNA dataset comprising samples from major ecosystems (terrestrial, freshwater, and marine) to attempt a global assessment of fungal diversity and community composition. We found the highest fungal diversities for terrestrial > freshwater > marine environments, and pronounced gradients of fungal diversity along temperature, salinity, and latitude in all ecosystems. We also identified the most abundant taxa in each of these ecosystems, mostly dominated by Ascomycota and Basidiomycota, except in freshwater rivers where Chytridiomycota dominated. Collectively, our analysis provides a global analysis of fungal diversity across all major environmental ecosystems, highlighting the most distinct order and ASVs (amplicon sequencing variants) by ecosystem, and thus filling a critical gap in the study of the Earth's mycobiome.

Seasonal shifts in Fe-acquisition strategies in Southern Ocean microbial communities revealed by metagenomics and autonomous sampling.

Iron (Fe) governs the cycling of organic carbon in large parts of the Southern Ocean. The strategies of diverse microbes to acquire the different chemical forms of Fe under seasonally changing organic carbon regimes remain, however, poorly understood. Here, we report high-resolution seasonal metagenomic observations from the region off Kerguelen Island (Indian Sector of the Southern Ocean) where natural Fe-fertilization induces consecutive spring and summer phytoplankton blooms. Our data illustrate pronounced, but distinct seasonal patterns in the abundance of genes implicated in the transport of different forms of Fe and organic substrates, of siderophore biosynthesis and carbohydrate-active enzymes. The seasonal dynamics suggest a temporal decoupling in the prokaryotic requirements of Fe and organic carbon during the spring phytoplankton bloom and a concerted access to these resources after the summer bloom. Taxonomic assignments revealed differences in the prokaryotic groups harbouring genes of a given Fe-related category and pronounced seasonal successions were observed. Using MAGs we could decipher the respective Fe- and organic substrate-related genes of individual taxa assigned to abundant groups. The ecological strategies related to Fe-acquisition provide insights on how this element could shape microbial community composition with potential implications on organic matter transformations in the Southern Ocean.

Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites.

Marine protists are major components of the oceanic microbiome that remain largely unrepresented in culture collections and genomic reference databases. The exploration of this uncharted protist diversity in oceanic communities relies essentially on studying genetic markers from the environment as taxonomic barcodes. Here we report that across 6 large scale spatio-temporal planktonic surveys, half of the genetic barcodes remain taxonomically unassigned at the genus level, preventing a fine ecological understanding for numerous protist lineages. Among them, parasitic Syndiniales (Dinoflagellata) appear as the least described protist group. We have developed a computational workflow, integrating diverse 18S rDNA gene metabarcoding datasets, in order to infer large-scale ecological patterns at 100% similarity of the genetic marker, overcoming the limitation of taxonomic assignment. From a spatial perspective, we identified 2171 unassigned clusters, i.e., Syndiniales sequences with 100% similarity, exclusively shared between the Tropical/Subtropical Ocean and the Mediterranean Sea among all Syndiniales orders and 25 ubiquitous clusters shared within all the studied marine regions. From a temporal perspective, over 3 time-series, we highlighted 39 unassigned clusters that follow rhythmic patterns of recurrence and are the best indicators of parasite community's variation. These clusters withhold potential as ecosystem change indicators, mirroring their associated host community responses. Our results underline the importance of Syndiniales in structuring planktonic communities through space and time, raising questions regarding host-parasite association specificity and the trophic mode of persistent Syndiniales, while providing an innovative framework for prioritizing unassigned protist taxa for further description.

Microbial iron and carbon metabolism as revealed by taxonomy-specific functional diversity in the Southern Ocean.

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.

Microbial iron metabolism as revealed by gene expression profiles in contrasted Southern Ocean regimes.

Iron (Fe) is a limiting nutrient in large regions of the ocean, but the strategies of prokaryotes to cope with this micronutrient are poorly known. Using a gene-specific approach from metatranscriptomics data, we investigated seven Fe-related metabolic pathways in microbial communities from high nutrient low chlorophyll and naturally Fe-fertilized waters in the Southern Ocean. We observed major differences in the contribution of prokaryotic groups at different taxonomic levels to transcripts encoding Fe-uptake mechanisms, intracellular Fe storage and replacement and Fe-related pathways in the tricarboxylic acid (TCA) cycle. The composition of the prokaryotic communities contributing to the transcripts of a given Fe-related pathway was overall independent of the in situ Fe supply, indicating that microbial taxa utilize distinct Fe-related metabolic processes. Only a few prokaryotic groups contributed to the transcripts of more than one Fe-uptake mechanism, suggesting limited metabolic versatility. Taxa-specific expression of individual genes varied among prokaryotic groups and was substantially higher for all inspected genes in Fe-limited as compared to naturally fertilized waters, indicating the link between transcriptional state and Fe regime. Different metabolic strategies regarding low Fe concentrations in the Southern Ocean are discussed for two abundant prokaryotic groups, Pelagibacteraceae and Flavobacteriaceae.

Diatoms shape the biogeography of heterotrophic prokaryotes in early spring in the Southern Ocean.

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.