Abstract

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