Climate genomics-Geoscientists, ecologists, and geneticists must reinforce their collaborations to confront climate change.

Geoscientists and ecologists alike must confront the impact of climate change on ecosystems and the services they provide. In the marine realm, major changes are projected in net primary and export production, with significant repercussions on food security, carbon storage, and climate system feedbacks. However, these projections do not include the potential for rapid linear evolution to facilitate adaptation to environmental change. Climate genomics confronts this challenge by assessing the vulnerability of ecosystem services to climate change. Because DNA is the primary biological repository of detectable environmentally selected mutations (showing evidence of change before impacts arise in morphological or metabolic patterns), genomics provides a window into selection in response to climate change, while also recording neutral processes deriving from stochastic mechanisms (Lowe et al., Trends in Ecology & Evolution, 2017; 32:141-152). Due to the revolution afforded by sequencing technology developments, genomics can now meet ecologists and climate scientists in a cross-disciplinary space fertile for collaborations. Collaboration between geoscientists, ecologists, and geneticists must be reinforced in order to combine modeling and genomics approaches at every scale to improve our understanding and the management of ecosystems under climate change. To this end, we present advances in climate genomics from plankton to larger vertebrates, stressing the interactions between modeling and genomics, and identifying future work needed to develop and expand the field of climate genomics.

Ocean-wide comparisons of mesopelagic planktonic community structures.

For decades, marine plankton have been investigated for their capacity to modulate biogeochemical cycles and provide fishery resources. Between the sunlit (epipelagic) layer and the deep dark waters, lies a vast and heterogeneous part of the ocean: the mesopelagic zone. How plankton composition is shaped by environment has been well-explored in the epipelagic but much less in the mesopelagic ocean. Here, we conducted comparative analyses of trans-kingdom community assemblages thriving in the mesopelagic oxygen minimum zone (OMZ), mesopelagic oxic, and their epipelagic counterparts. We identified nine distinct types of intermediate water masses that correlate with variation in mesopelagic community composition. Furthermore, oxygen, NO3- and particle flux together appeared as the main drivers governing these communities. Novel taxonomic signatures emerged from OMZ while a global co-occurrence network analysis showed that about 70% of the abundance of mesopelagic plankton groups is organized into three community modules. One module gathers prokaryotes, pico-eukaryotes and Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) from oxic regions, and the two other modules are enriched in OMZ prokaryotes and OMZ pico-eukaryotes, respectively. We hypothesize that OMZ conditions led to a diversification of ecological niches, and thus communities, due to selective pressure from limited resources. Our study further clarifies the interplay between environmental factors in the mesopelagic oxic and OMZ, and the compositional features of communities.

Plankton biogeography in the 21st century and impacts of climate change: advances through genomics.

This article summarizes recent advances in our knowledge of plankton biogeography obtained by genomic approaches and the impacts of global warming on it. Large-scale comparison of the genomic content of samples of different plankton size fractions revealed a partitioning of the oceans into genomic provinces and the impact of major oceanic currents on them. By defining ecological niches, these provinces are extrapolated to all oceans, with the exception of the Arctic Ocean. By the end of the 21st century, a major restructuring of these provinces is projected in response to a high emission greenhouse gas scenario over 50% of the surface of the studied oceans. Such a restructuring could lead to a decrease in export production by 4%. Finally, obtaining assembled sequences of a large number of plankton genomes defining this biogeography has allowed to better characterize the genomic content of the provinces and to identify the species structuring them. These genomes similarly enabled a better description of potential future changes of plankton communities under climate change.

Cet article résume des avancées récentes dans nos connaissances sur la biogéographie du plancton obtenues par des approches de génomiques ainsi que les impacts du réchauffement climatique sur celle-ci. La comparaison à large échelle du contenu génomique d'échantillons de différentes fractions de taille de plancton a révélé un partitionnement des océans en provinces génomiques ainsi que l'impact des principaux courants océaniques sur celles-ci. En définissant des niches écologiques, ces provinces sont extrapolées à l'ensemble des océans à l'exception de l'océan Arctique. D'ici la fin du XXI e siècle, une restructuration majeure de ces provinces est projetée en réponse à un scénario de fortes émissions de gaz à effet de serre sur 50 % de la surface des océans étudiés. Une telle restructuration pourrait engendrer une diminution de 4 % de la production exportée. L'obtention de séquences assemblées d'un grand nombre de génomes de plancton définissant cette biogéographie a permis de mieux caractériser le contenu génomique des provinces et d'identifier les espèces les structurant. Ces génomes ont aussi permis de mieux caractériser les futurs changements potentiels de communautés de plancton sous changement climatique.

Genomic adaptation of the picoeukaryote Pelagomonas calceolata to iron-poor oceans revealed by a chromosome-scale genome sequence.

The smallest phytoplankton species are key actors in oceans biogeochemical cycling and their abundance and distribution are affected with global environmental changes. Among them, algae of the Pelagophyceae class encompass coastal species causative of harmful algal blooms while others are cosmopolitan and abundant. The lack of genomic reference in this lineage is a main limitation to study its ecological importance. Here, we analysed Pelagomonas calceolata relative abundance, ecological niche and potential for the adaptation in all oceans using a complete chromosome-scale assembled genome sequence. Our results show that P. calceolata is one of the most abundant eukaryotic species in the oceans with a relative abundance favoured by high temperature, low-light and iron-poor conditions. Climate change projections based on its relative abundance suggest an extension of the P. calceolata habitat toward the poles at the end of this century. Finally, we observed a specific gene repertoire and expression level variations potentially explaining its ecological success in low-iron and low-nitrate environments. Collectively, these findings reveal the ecological importance of P. calceolata and lay the foundation for a global scale analysis of the adaptation and acclimation strategies of this small phytoplankton in a changing environment.

Genomic evidence for global ocean plankton biogeography shaped by large-scale current systems.

Biogeographical studies have traditionally focused on readily visible organisms, but recent technological advances are enabling analyses of the large-scale distribution of microscopic organisms, whose biogeographical patterns have long been debated. Here we assessed the global structure of plankton geography and its relation to the biological, chemical, and physical context of the ocean (the 'seascape') by analyzing metagenomes of plankton communities sampled across oceans during the Tara Oceans expedition, in light of environmental data and ocean current transport. Using a consistent approach across organismal sizes that provides unprecedented resolution to measure changes in genomic composition between communities, we report a pan-ocean, size-dependent plankton biogeography overlying regional heterogeneity. We found robust evidence for a basin-scale impact of transport by ocean currents on plankton biogeography, and on a characteristic timescale of community dynamics going beyond simple seasonality or life history transitions of plankton.

Oceans are brimming with life invisible to our eyes, a myriad of species of bacteria, viruses and other microscopic organisms essential for the health of the planet. These 'marine plankton' are unable to swim against currents and should therefore be constantly on the move, yet previous studies have suggested that distinct species of plankton may in fact inhabit different oceanic regions. However, proving this theory has been challenging; collecting plankton is logistically difficult, and it is often impossible to distinguish between species simply by examining them under a microscope. However, within the last decade, a research schooner called Tara has travelled the globe to gather thousands of plankton samples. At the same time, advances in genomics have made it possible to identify species based only on fragments of their DNA sequence. To understand the hidden geography of plankton communities in Earth's oceans, Richter et al. pored over DNA from the Tara Oceans expedition. This revealed that, despite being unable to resist the flow of water, various planktonic species which live close to the surface manage to occupy distinct, stable provinces shaped by currents. Different sizes of plankton are distributed in different sized provinces, with the smallest organisms tending to inhabit the smallest areas. Comparing DNA similarities and speeds of currents at the ocean surface revealed how these might stretch and mix plankton communities. Plankton play a critical role in the health of the ocean and the chemical cycles of planet Earth. These results could allow deeper investigation by marine modellers, ecologists, and evolutionary biologists. Meanwhile, work is already underway to investigate how climate change might impact this hidden geography.

Functional repertoire convergence of distantly related eukaryotic plankton lineages abundant in the sunlit ocean.

Marine planktonic eukaryotes play critical roles in global biogeochemical cycles and climate. However, their poor representation in culture collections limits our understanding of the evolutionary history and genomic underpinnings of planktonic ecosystems. Here, we used 280 billion Tara Oceans metagenomic reads from polar, temperate, and tropical sunlit oceans to reconstruct and manually curate more than 700 abundant and widespread eukaryotic environmental genomes ranging from 10 Mbp to 1.3 Gbp. This genomic resource covers a wide range of poorly characterized eukaryotic lineages that complement long-standing contributions from culture collections while better representing plankton in the upper layer of the oceans. We performed the first, to our knowledge, comprehensive genome-wide functional classification of abundant unicellular eukaryotic plankton, revealing four major groups connecting distantly related lineages. Neither trophic modes of plankton nor its vertical evolutionary history could completely explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years.

Universal and idiosyncratic characteristic lengths in bacterial genomes.

In condensed matter physics, simplified descriptions are obtained by coarse-graining the features of a system at a certain characteristic length, defined as the typical length beyond which some properties are no longer correlated. From a physics standpoint, in vitro DNA has thus a characteristic length of 300 base pairs (bp), the Kuhn length of the molecule beyond which correlations in its orientations are typically lost. From a biology standpoint, in vivo DNA has a characteristic length of 1000 bp, the typical length of genes. Since bacteria live in very different physico-chemical conditions and since their genomes lack translational invariance, whether larger, universal characteristic lengths exist is a non-trivial question. Here, we examine this problem by leveraging the large number of fully sequenced genomes available in public databases. By analyzing GC content correlations and the evolutionary conservation of gene contexts (synteny) in hundreds of bacterial chromosomes, we conclude that a fundamental characteristic length around 10-20 kb can be defined. This characteristic length reflects elementary structures involved in the coordination of gene expression, which are present all along the genome of nearly all bacteria. Technically, reaching this conclusion required us to implement methods that are insensitive to the presence of large idiosyncratic genomic features, which may co-exist along these fundamental universal structures.