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Functional Redundancy of the Global Ocean Microbiome

Periodic Reporting for period 1 - FROM (Functional Redundancy of the Global Ocean Microbiome)

Okres sprawozdawczy: 2022-04-01 do 2024-03-31

This proposal relates to a recent debate of microbiology. Functional redundancy supposes that many taxa can realize the
same functions. In this scenario, the composition of microbial communities could appear as a bad predictor of their effects on
ecosystems. Functional redundancy among microbes has been suggested but also disproven, growing in a limiting debate
for microbiology. Our project proposes an overview of microbial functions to answer to this debate. The innovation in our
project consists in studying the ecology and redundancy of functions inferred by various methods. We will use state-of-the
art microbiome datasets that spans the global ocean, enabling to study the impact of geographic scales on redundancy. The
host and the candidate will bring together their complementary expertise on omics, statistics, microbes’ morphology, nutrition
and interactions to compare for the first time the functionality of all microbial domains across the global ocean. Inferred
functions will be analyzed against microbial taxonomy, environmental selection from abiotic variables and dispersal across
the ocean to study their redundancy and ecological patterns. Novel cross-disciplinary tools will be developed that will expand
the outreach of our project to research in omics (e.g. bioinformatics, computational biology), biogeochemistry, modelling,
evolution or global changes. Morpho-trophic features of protistan taxa will be collected into a novel database that will
represent their functional diversity. Finally, an innovative functional characterization of ecological networks will be developed
to unveil the interplay between microbial interaction networks and environmental conditions. Researchers and policy-makers
studying how microbes affects natural, engineered, or future ecosystems, will benefit from our project that represents a
major leap forward for microbiology and functional ecology.
The main scientific objectives of the project “Functional Redundancy of the Global Ocean Microbiome (FROM)” were to develop approaches to study microbial functional redundancy and diversity and explain their patterns in the global ocean. The ideas leading to the development of FROM were first summarized in an opinion/review piece we called: “Microbial functional diversity and redundancy: moving forward”. In this piece, we review the state of the field of microbial functional ecology, we identify limiting factors and outline a framework to circumvent them. Finally, we detail ensuing perspectives for the field. We then applied this new found framework using public data, namely: a) a collection of prokaryotic genomes (Paoli et al., 2022), b) methods to predict biogeochemically relevant traits from genomes (Zhou et al., 2022), c) metagenomes and meta-transcriptomes (Sunagawa et al., 2020), and d) an unpublished collection of prokaryotic genomes, metagenomes and meta-transcriptomes from the ICM-CSIC (host institution) (http://bbmo.icm.csic.es/(odnośnik otworzy się w nowym oknie)) to compute microbial functional diversity and redundancy in the global ocean. We first evidence that potential and expressed microbial redundancy generally correlate in the ocean, suggesting that, when present, microbes express their traits. We then evidence that deeper layers harbor more versatile microbes which leads to a lowering of redundancy in deep microbiomes. In the surface ocean, functional diversity was homogeneous but redundancy was markedly lower between the temperate and the polar area. Polar areas harbor lower microbial richness, higher dominance from opportunistic taxa, and larger community turnover. Finally, using machine learning and earth model projections, we predict further losses of redundancy at the horizon of 2100, notably in surface temperate and the equatorial Pacific Ocean. Being able to quantify microbes' functional diversity and redundancy, we are now poised to test the significance of these metrics for the functioning of present and future ecosystems facing climate change.
To apply this method to microbial eukaryotes, we started an international working group on Protists Trait Annotation. The aims of this working group are: 1) to identify a key set of traits representing the ecological functions of protists and their roles in ecosystems. 2) To annotate all known protistan taxa with these traits, and find experts to perform and supervise this task. 3) To analyze and explain patterns of protists functional ecology across biomes. In a preliminary approach, a MSc student (Louise Pietri from Aix-Marseille Université, France) joined FROM to annotate the protist taxa in the collection of oceanic metabarcoding datasets (Vaulot et al., 2022). After a successful work of annotation, Louise then explored patterns of protist traits in the ocean. In the samples analyzed, we highlight that the majority of oceanic protists harbor simple morphology (round naked cells), are able to swim in order to predate or avoid predation, they also generally lack of defense appendages and are unable to perform dormancy. A promising result was the apparent correlation between protists feeding strategy and cell size with estimations of oceanic carbon bottom export, suggesting that this key ecosystem process could be predicted from functionally characterized marine protistan communities. The next step with this approach is to predict and explain patterns microbial eukaryotes functional redundancy in the ocean. Another underlying project is using the traits of marine protists to functionally characterize network-predicted interactions in marine microbiome and potentially unveil general rules of microbial interactions in time and space. This project will be offered as new MSc study in autumn 2024.
Our piece on “Microbial functional diversity and redundancy: moving forward” work is currently under-review in the journal FEMS Microbiology Reviews, a preprint is available in the EcoEvoRXIV server (https://doi.org/10.32942/X2DC85(odnośnik otworzy się w nowym oknie)). Manuscripts for the publication of other results are still in preparation. However, most results have been presented at local, national, and international conferences, leading to ongoing collaborations that will lead to further publications. The pipelines developed within FROM are made public on Github (github.com/pjmramond). Currently, the research carried did not have an impact on industries. However, the axes of research, if carried over a mid-to-longer term could lead to impact on industries involved in waste-water treatment or algal biomass production. Establishing and predicting key microbial features could also guide decision-makers in terms of the impact of climate change on marine microbiomes and ecosystems.
Summary of the project FROM and its outlined perspectives
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