Metabolism of microbiomes in a changing Arctic Ocean

The world’s oceans are of utmost importance for us humans: they are a source of food \nand half of the oxygen we breathe, they act as climate regulators, trade routes, tourism attractions, \nand harbor an incredible diversity of life. The Arctic Ocean represents a particular \nocean, with acute variations of temperatures, ice and solar radiation regimes throughout the \nyear, and a strong terrestrial signature imparted by its immense watershed. But the oceans \nare now under threat of a changing climate. The polar oceans are especially susceptible to \nthese changes with already dramatic visible consequences. The most visible consequence in \nthe Arctic Ocean is a continuous loss of sea ice with impact on albedo, solar radiation regimes \non the water surface, phytoplankton growth and primary productivity. The Arctic is also receiving \nincreasing amounts of freshwater, leading to a freshening, disturbing the water column \nstratification, and increasing the load of organic matter from terrestrial origin. All these perturbations \nprofoundly modify the sources and dynamics of organic and inorganic matter in the \nArctic Ocean, perturbing the Arctic Ocean biogeochemical cycles. Given that microbial life is \nat the base of cycling this organic and inorganic matter, microbes play pivotal roles by controlling \nbiogeochemical cycles and forming the base of the food web. Specifically, the diversity \nof metabolic processes carried out by microbes determines how they interact with and shape \ntheir environment. Despite the importance of understanding microbial metabolism in a rapidly \nchanging Arctic Ocean, our knowledge of the microbial processes that distinguish the Arctic \nOcean from the rest of the global oceans and how they are linked to the changing Arctic Ocean \nbiogeochemical cycles is still very fragmented. \nIn this thesis, I undertook to address the lack of knowledge about the metabolism of the \nArctic Ocean microbiomes by tackling two fundamental questions: (i) What are the specificities \nand phylogenetic diversity of microbial metabolism in the Arctic Ocean compared to the other \nworld oceans? (ii) What are the relationships between the Arctic Ocean microbial metabolic \nspecificities and their biogeochemical environment? \nI first discovered that metabolic pathways for the degradation of aromatic compounds were \nenriched and expressed in the Canada Basin of the Arctic Ocean compared to the rest of the \nglobal ocean, in particular in the subsurface waters where organic matter of terrestrial origin \naccumulates. The capacity to degrade aromatic compound from terrestrial origin was phylogenetically \nconcentrated in Rhodspirillales. These Rhodospirillales were enriched in aromatic \ncompound degradation genes compared to close relatives from other oceans and their geographic \ndistribution was restricted to the Arctic Ocean. These results suggest that the capacity to degrade \naromatic compounds of terrestrial origin may be an adaptive trait of some Arctic Ocean \nmicrobial taxa. Furthermore, the aromatic-metabolizing bacteria may become more prominent \nas organic matter inputs from land to ocean continue to rise with climate change, potentially \nimpact the Arctic Ocean biogeochemical cycles. \nIn the second part of this thesis, I focused on the metabolism of neutral lipids, used to accumulate \nenergy and carbon reserves. Within the global ocean, I discovered that the metabolism \nof neutral lipids was enriched in the microbial communities of the Arctic Ocean. In the photic \nzone, eukaryotic phototrophs dominated the synthesis of neutral lipids. I also discovered a \nlarge diversity of bacterial taxa able to degrade but not produce neutral lipids, suggesting that \nphotosynthetic-based production of neutral lipids in eukaryotes may serve as an important carbon \nsource for the heterotrophic bacterial community. Bacteria were the main producers in the \naphotic zone and were equipped with a di↵erent set of enzymes targeting di↵erent compounds \ndepending on their location within the water column. This study shows that the storage of \nneutral lipids may be a selective advantage for prokaryotes and picoeukaryotes in a context of \nextreme variations in energy and nutrients sources such as in the Arctic Ocean. In addition, \nI propose that, similarly to lipids from eukaryotic phototrophs sustaining the food web during \nthe summer months, neutral lipids from prokaryotic origin may play an important role in sustaining \nthe food web during the dark winter months. \nFinally, I undertook a global ocean study to unravel the metabolic genes and pathways \nfavored by the microbiomes of the Arctic Ocean. I confirmed the importance of aromatic \ncompound degradation and neutral lipid metabolism. But I also uncovered a myriad of other \nmetabolic processes favored by the microbiomes of the Arctic Ocean compared to other oceanic \nzones. In particular, in the photic zone of the Arctic Ocean, I discovered the prevalence of genes \nand pathways involved in the metabolism of glycans that might be involved in cold adaptation \nmechanisms. Importantly, I highlighted correspondences between the genes and pathways favored \nby the Arctic Ocean microbiomes and the composition and transformations of dissolved \norganic matter. Specifically, I found an enrichment in transformations involving sugars moieties \nin the photic zone and a strong aromaticity signature in the dissolved organic matter \nof the fluorescent dissolved organic matter maximum. These results show that the distinct \nmetabolism of the Arctic Ocean microbiomes imprint the composition of the dissolved organic \nmatter, uniquely influencing the Arctic Ocean biogeochemical cycles. \nThis thesis represents the first work to explore the metabolism of the Arctic Ocean microbiomes \nin such a comprehensive fashion. Not only does this thesis systematically uncover a \nmultitude of metabolic processes of importance for the Arctic Ocean microbiomes, but it also \nbrings new discoveries on their biogeography, ecological context, and phylogenetic diversity \nacross prokaryotes and picoeukaryotes. Moreover, this thesis highlights the importance of these \nprocesses by linking them to the composition and transformation of dissolved organic matter, \nand hence biogeochemical cycles. As such, this thesis will serve as a base to guide experimental \nand field work that will quantify the role of microbiomes in the biogeochemical cycles of the \nArctic Ocean. This will have important implications to understand and quantify how climate \nchange perturbs Arctic Ocean ecosystems.

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