Assembly processes and functional diversity of marine protists and their rare biosphere.

BACKGROUND: The mechanisms shaping the rare microbial biosphere and its role in ecosystems remain unclear. We developed an approach to study ecological patterns in the rare biosphere and use it on a vast collection of marine microbiomes, sampled in coastal ecosystems at a regional scale. We study the assembly processes, and the ecological strategies constituting the rare protistan biosphere. Using the phylogeny and morpho-trophic traits of these protists, we also explore their functional potential. RESULTS: Taxonomic community composition remained stable along rank abundance curves. Conditionally rare taxa, driven by selection processes, and transiently rare taxa, with stochastic distributions, were evidenced along the rank abundance curves of all size-fractions. Specific taxa within the divisions Sagenista, Picozoa, Telonemia, and Choanoflagellida were rare across time and space. The distribution of traits along rank abundance curves outlined a high functional redundancy between rare and abundant protists. Nevertheless, trophic traits illustrated an interplay between the trophic groups of different size-fractions. CONCLUSIONS: Our results suggest that rare and abundant protists are evolutionary closely related, most notably due to the high microdiversity found in the rare biosphere. We evidenced a succession of assembly processes and strategies of rarity along rank abundance curves that we hypothesize to be common to most microbiomes at the regional scale. Despite high functional redundancy in the rare protistan biosphere, permanently rare protists were evidenced, and they could play critical functions as bacterivores and decomposers from within the rare biosphere. Finally, changes in the composition of the rare protistan biosphere could be influenced by the trophic regime of aquatic ecosystems. Our work contributes to understanding the role of rare protists in microbiomes.

Phytoplankton taxonomic and functional diversity patterns across a coastal tidal front.

Oceanic physics at fine scale; e.g. eddies, fronts, filaments; are notoriously difficult to sample. However, an increasing number of theoretical approaches hypothesize that these processes affect phytoplankton diversity which have cascading effects on regional ecosystems. In 2015, we targeted the Iroise Sea (France) and evidenced the setting up of the Ushant tidal front from the beginning of spring to late summer. Seawater samples were taken during three sampling cruises and DNA-barcoding allowed us to investigate patterns of eukaryotic phytoplankton diversity across this front. First focusing on patterns of taxonomic richness, we evidenced that the front harbored a hotspot of eukaryotic phytoplankton diversity sustained throughout summer. We then detail the ecological processes leading to the formation of this hotspot by studying shifts in community composition across the Iroise Sea. Physical mixing mingled the communities surrounding the front, allowing the formation of a local ecotone, but it was cycles of disturbances and nutrient inputs over the front that allowed a decrease in competitive exclusion, which maintained a higher diversity of rare phytoplankton taxa. These processes did not select a specific ecological strategy as inferred by a trait approach coupled to our taxonomic approach. Instead the front favored higher richness within widespread strategies, resulting in functional redundancy. We detail how fine-scale ocean physics affect phytoplankton diversity and suppose that this interplay is a major control on regional ecosystems.

Species specific gene expression dynamics during harmful algal blooms.

Harmful algal blooms are caused by specific members of microbial communities. Understanding the dynamics of these events requires comparing the strategies developed by the problematic species to cope with environmental fluctuations to the ones developed by the other members of the community. During three consecutive years, the meta-transcriptome of micro-eukaryote communities was sequenced during blooms of the toxic dinoflagellate Alexandrium minutum. The dataset was analyzed to investigate species specific gene expression dynamics. Major shifts in gene expression were explained by the succession of different species within the community. Although expression patterns were strongly correlated with fluctuation of the abiotic environment, and more specifically with nutrient concentration, transcripts specifically involved in nutrient uptake and metabolism did not display extensive changes in gene expression. Compared to the other members of the community, A. minutum displayed a very specific expression pattern, with lower expression of photosynthesis transcripts and central metabolism genes (TCA cycle, glucose metabolism, glycolysis…) and contrasting expression pattern of ion transporters across environmental conditions. These results suggest the importance of mixotrophy, cell motility and cell-to-cell interactions during A. minutum blooms.

Coupling between taxonomic and functional diversity in protistan coastal communities.

The study of protistan functional diversity is crucial to understand the dynamics of oceanic ecological processes. We combined the metabarcoding data of various coastal ecosystems and a newly developed trait-based approach to study the link between taxonomic and functional diversity across marine protistan communities of different size-classes. Environmental DNA was extracted and the V4 18S rDNA genomic region was amplified and sequenced. In parallel, we tried to annotate the operational taxonomic units (OTUs) from our metabarcoding dataset to 30 biological traits using published and accessible information on protists. We then developed a method to study trait correlations across protists (i.e. trade-offs) in order to build the best functional groups. Based on the annotated OTUs and our functional groups, we demonstrated that the functional diversity of marine protist communities varied in parallel with their taxonomic diversity. The coupling between functional and taxonomic diversity was conserved across different protist size classes. However, the smallest size-fraction was characterized by wider taxonomic and functional groups diversity, corroborating the idea that nanoplankton and picoplankton are part of a more stable ecological background on which larger protists and metazoans might develop.