DS01 - Gestion sobre des ressources et adaptation au changement climatique

Cross-scale analysis of adaptation to iron depletion in a key phytoplanktonic organism, in the context of global change – CINNAMON

How do iron availability and temperature affect marine phytoplankton diversity and distribution?

Due to its abundance, ubiquity and the availability of many isolates and genomes, the marine cyanobacterium Synechococcus is a relevant micro-organism to understand the effects of environmental changes, and in particular temperature and iron availability.

Adaptation mechanisms of marine cyanobacteria to iron deficiency and temperature stress

The oceans are particularly affected by the global change, which causes an increase in the temperature of the sea water but also of the surface of areas poor in iron, an element that already limits the growth of phytoplankton in nearly 35% of the world's ocean. This raises the question of the ability of phytoplankton to adapt to these new conditions and of the consequences of these changes on the biological pump. In this context, the recent discovery that CRD1, a lineage of the marine cyanobacterium Synechococcus, dominates in iron-poor waters and that 3 genetically distinct populations (CRD1-A to C) occupy different thermal niches, constitutes a unique opportunity to study the combined effects of iron deficiency and temperature on phytoplankton at all levels of organization, from genes to ecosystem. <br />The main objectives of the CINNAMON project are to: i) validate the presence of distinct ecotypes with respect to iron and/or temperature by determining the growth optima and limits for these parameters of 3 CRD1 strains, ii) to identify the genetic basis of this adaptation by a comparative genomic approach using the numerous genomes of marine cyanobacteria, representative of various environments, iii) to use meta-omic data from expeditions such as Tara Oceans, in order to validate the observations made in the laboratory but also to identify new genes potentially involved in the ability of these ecotypes to adapt to iron-depleted waters and to different temperature niches. Overall, this project should make it possible to better predict the respective adaptability of the different lineages, and therefore their future distribution and dynamics in a changing ocean.

The CINNAMON project uses a systems biology approach to characterize and model the main mechanisms of acclimation (physiology) and adaptation (evolution) involved in the differential response of Synechococcus ecotypes to iron deficiency and temperature variations. First, we study the physiological response (regulation of photosynthetic activity, modification of the transcriptome, lipid composition, pigment content, etc.) of 3 CRD1 strains as well as representative strains of the four other major Synechococcus lineages, acclimated to different iron concentrations and/or temperatures, to better understand the mechanisms involved in the response to these two stresses in different lineages of the Synechococcus genus. In parallel, comparative studies of available Synechococcus genomes will elucidate the genetic basis of the response to these environmental factors. The combination of these genomic analyses with transcriptomic data acquired under +Fe/-Fe conditions and/or at different temperatures will make it possible to identify genes specific of CRD1 and/or differentially regulated in response to iron deficiency or thermal variations. The function of these genes will then be characterized by looking at the effect of their inactivation by mutagenesis on cell physiology, in order to better understand the mechanisms involved in the response to these stresses. Finally, the role of these genes will be studied in an environmental context, by looking at their presence and their expression level in natural populations of Synechococcus through the analysis of metagenomes and metatranscriptomes, generated from seawater samples harvested during oceanographic expeditions, such as Tara Oceans.

Comparative physiology studies of Synechococcus strains representative of dominant lineages in iron-depleted or replete environments (CRD1 vs I-IV clades), acclimated to different temperatures, have allowed us i) to validate the existence of distinct thermotypes within the CRD1 clade, i.e. with different thermal tolerance ranges and ii) to reveal interesting features of the photosynthetic apparatus of CRD1 strains and in particular their ability to repair the damages caused to this complex at the boundary limit of their thermal growth range. Genomic comparisons have also identified genetic specificities of CRD1 compared to other clades, which may be involved in adaptation to iron deficiency. This includes the reduction of the number of genes encoding iron-rich proteins, the use of alternative proteins using other metals than iron as co-factors or the amplification of gene families coding for proteins potentially involved in the transport, assimilation and storage of iron. On the other hand, the comparisons between warm and cold thermotypes revealed only a few specific genes of one group or the other, with the exception of desaturases allowing to adjust the fluidity of the photosynthetic membranes, the adaptation to thermal niches implying rather modifications of the gene sequence. Finally, the analysis of environmental data has revealed genes that are specifically present or absent in the iron-poor niches, and in particular many uncharacterized genes that constitute good candidates for going further in understanding of the mechanisms of adaptation to iron deficiency of Synechococcus CRD1 and phytoplankton in general.

Understanding the impact of Fe limitation responds to a societal claim, as the general public is increasingly aware of the importance of preserving ecosystems, especially marine areas, and decision-makers need effective tools for oceans management. In this context, the results of the CINNAMON project should provide a better understanding of the ability of marine phytoplankton to cope with ongoing climate changes and how they will affect the structure and population dynamics of this basal compartment of marine ecosystems. Another perspective of the CINNAMON project is the possibility of using the Synechococcus CRD1 ecotypes and/or their specific genes as biomarkers for monitoring the expansion of iron-poor regions, iron limitation being particularly difficult to assess by chemical approaches.

Three papers have been published for the time being from the results of CINNAMON, one of which describes the effect on picocyanobacterial populations of a local iron enrichment induced by the Marquesas Islands, located in the iron-poorest region of the wo

Oceans are particularly affected by the global change, which notably causes an increase in seawater temperature and an expansion of iron (Fe)-poor areas, whilst Fe depletion is already impairing phytoplankton growth in as much as 35 % of the global ocean. This raises the questions of the capacity of local marine phytoplanktonic populations to adapt to these harsh conditions and of the consequences of Fe depletion on the ocean ability to sequester CO2 via the biological carbon pump. In this context, the recent discovery of one clade (CRD1) of the marine cyanobacterium Synechococcus predominating in low-Fe niches, with three genetically distinct populations displaying different temperature ranges, constitutes a unique opportunity to unveil the combined effects of Fe depletion and temperature on phytoplankton at all scales of organization from the gene to the ecosystem.
The CINNAMON project will use a systems biology approach, combining laboratory and field work, to characterize and model the main acclimation (physiological) and adaptation (evolutionary) mechanisms involved in the differential responses of Synechococcus ecotypes to Fe limitation and temperature variations, with the goal to better predict their respective adaptability, and hence future distribution and dynamics in a changing environment. First, we will validate the occurrence of distinct Fe and/or temperature ecotypes within the CRD1 clade, notably by delineating the growth optima and boundary limits for Fe and temperature of representative strains. In parallel, the comparison i) of genomes of marine picocyanobacteria (about 60 Synechococcus genomes, including at least one for each CRD1 genotype and 2 low-Fe Prochlorococcus metagenomes) and ii) of transcriptomes from different CRD1 and control strains generated in response to +Fe/-Fe, should allow us to decipher the genetic basis of their specific adaptability to changes in temperature and Fe availability. These data will also be integrated into co-expression and metabolic networks in order to determine the respective role of metabolic vs. regulatory pathways in the differential behavior of the tested strains when subjected to Fe depletion and high/low temperature. A last approach will consist in using meta-omics data from major global ocean surveys (Tara-Oceans, Tara-Polar Circle, Tara-Pacific and Malaspina expeditions) covering a wide range of oceanic regimes to validate at the population level the observations made on representative strains, but also to identify additional genes and biosynthetic pathways potentially responsible for the capacity of these ecotypes to adapt to cold or warm, low-Fe regions of the world ocean. Altogether, this cross-scales approach from the genes to the global ocean should allow us to delineate a limited set of ecotype- and/or niche-specific genes that are differentially expressed in response to Fe availability. Such genes will constitute privileged targets for further functional analyses, including gene inactivation followed by physiological characterization of mutants, to better understand molecular processes underlying adaptation to low Fe niches.
The CINNAMON project is both ambitious by the extent and variety of analyses that will be made and innovative since results will not be limited to a model Synechococcus strain, but will take into account the ecotypic variability within this major component of the oceanic ecosystem. Results will thus be of both evolutionary and ecological interest as they should allow us to better understand i) how iron availability has driven genetic diversification within picocyanobacteria, but also ii) the consequences of this diversification on the community composition and dynamics of these key organisms, in the context of global change. A major societal goal of the project will be to raise awareness among general public about the impact of global change on marine biodiversity and to provide tools to stakeholders to monitor these effects.

Project coordinator

Madame Laurence Garczarek (Adaptation et Diversité en Milieu Marin)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

AD2M Adaptation et Diversité en Milieu Marin
LOMIC Laboratoire d'Océanographie Microbienne
LS2N (ex LINA) Laboratoire des Sciences du Numérique de Nantes
ABIMS Plateforme ABIMS (Analysis Bioinformatics for Marine Science)

Help of the ANR 449,924 euros
Beginning and duration of the scientific project: December 2017 - 36 Months

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