Synechococcus as a model genus for studying adaptation of marine phytoplankton to environmental changes – SAMOSA

The SAMOSA project rests on the development of a systems biology approach. First, we will study the biological response (regulation of photosynthetic activity, modification of transcriptome, proteome, lipid composition, etc.) of a model strain to various key environmental stresses (high light, ultraviolet, high and low temperature). These data will allow us to build a first global gene regulation network. The effect of high light and temperature will then be studied in several other strains, representative of the 4 dominant genetic groups (ecotypes) in the field, with the goal to determine responses and mechanisms specific of given stress and/or taxonomical groups within the Synechococcus genus.
At the same time, systematic comparative studies of 54 marine Synechococcus genomes will allow us to elucidate genetic bases of the adaptive response specific to various environmental factors. By comparing genomic and transcriptomic data, it will be possible to delineate genes specific of the different ecotypes and involved in the response to variations in environmental conditions. The function of these genes will then be characterized by looking at the effect of their inactivation on the cell physiology, with the aim to decipher mechanisms raised in response to stress. At last, the role of these genes will be studied in an environmental context by examining their occurrence and expression levels in field Synechococcus populations, using metagenomes and metatranscriptomes obtained from seawater samples collected during the TARA-Oceans circumnavigation cruise.

The comparison of 12 strains representative of the main genetic groups (3 strains for each) have allowed us to enlighten notable differences between these ecotypes, in particular with regard to temperature ranges at which these strains can grow, which agrees well with the latitude at which they were isolated. Analysis of the response to abrupt variations of environmental parameters (high light, UV, high/low temperature) has also revealed contrasted physiological responses both between ecotypes and between stress types.
The comparison of 97 picocyanobacterial genomes, including 32 now ones assembled and annotated in the framework of SAMOSA, has allowed us to identify both core gene repertoires and sets of genes specific of one group or shared by several groups of strains, the latter genes being good candidates to have a role in the adaptation to specific environmental conditions.
At last the diversity and distribution of Synechococcus at the global ocean scale has been determined by analyzing 111 metagenomes sampled during the TARA-Oceans cruise, using a marker gene with high resolution, allowing a good discrimination of the various genetic groups within this genus. These data have notably allowed to unveil the presence of groups whose abundance was so far widely underestimated, to identify novel groups for which there are no cultured representatives, and to delineate environmental conditions in which these different populations preferentially live.

Data generated in the framework of the SAMOSA project will be used to build a model of gene regulation network that will allow one to predict the capacity of the different genetic groups of a major genus of marine phytoplancton to alterations of the environment, notably woth regard to temperature and UV radiations rises known to result from the ongoing climate change.
This project could also lead to the characterization of genes potentially important for understanding the physiology of terrestrial plants, which directly descend from cyanobacteria, and/or to novel genes of biotechnological potential (e.g., involved in the biosynthetic pathway of lipids, a component of biofuels).

An article has recently been published in the prestigious journal « Science » notably describing changes occurring in the composition of Synechococcus populations occurring during the transport of water masses off the South coast of Africa traveling from the Indian Ocean to the South Atlantic (Agulhas rings). Another paper describing the major role of Synechococcus in structuring communities involved in carbon export has been submitted to Nature. Furthermore, a third paper describing the method that we used to assemble 32 new Synechococcus genomes id currently in revisions in BMC Bioinformatics. At last, several communications have been made in international congresses reporting the first results of the SAMOSA project.

Oceans are particularly affected by global change, which can cause e.g. increases in average sea temperature and in UV radiation fluxes onto ocean surface or a shrinkage of nutrient-rich areas. This raises the question of the capacity of marine photosynthetic microorganisms to cope with these environmental changes both at short term (physiological plasticity) and long term (e.g. gene alterations or acquisitions causing changes in fitness in a specific niche). Synechococcus cyanobacteria are among the most pertinent biological models to tackle this question, because of their ubiquity and wide abundance in the field, which allow them to be studied at all levels of organization from genes to the global ocean.

In SAMOSA, we plan to develop a systems biology approach to characterize and model the main acclimation (i.e., physiological) and adaptation (i.e. evolutionary) mechanisms involved in the differential responses of Synechococcus clades/ecotypes to environmental fluctuations, with the goal to better predict their respective adaptability, and hence dynamics and distribution, in the context of global change. First, we will measure, on synchronized and asynchronized cultures of the model Synechococcus strain WH7803, the effects of a variety of environmental stresses (high light, high and low temperature, UV exposure) on the whole transcriptome and a number of key physiological processes. These data, complemented with published data on oxidative and nutrient stress, will allow us to build a first global gene regulation network. Using the same approach, we will then study the effects of high light and temperature stresses on four additional Synechococcus strains, representative of the most abundant clades in the field, with the aim to unveil ecotype-specific responses. This will allow us to add subnetworks to the global gene regulation model that will translate the extent of ecotypic variability of the stress response within the Synechococcus genus.

In parallel, systematic comparisons of the 42 marine Synechococcus genomes available, including 2 to 10 strains for each clade, will allow us to identify the ecotype-specific core genomes. Knowledge of these gene sets should allow us to decipher the genetic basis of specific adaptive responses to changes in environmental factors among ecotypes. By combining comparative genomics and transcriptomics analyses, we expect to delineate a limited set of genes that are both ecotype-specific and differentially regulated in response to one or several specific stresses. Such genes will constitute privileged targets for further functional analyses, including gene knockout approaches followed by physiological characterization of the mutants. The role of these genes in stress adaptation of Synechococcus ecotypes will be further checked by screening metagenomes and metatranscriptomes from various oceanic regions and depths showing contrasted environmental parameters, which we will get from the TARA-Oceans cruise and other sources.

The SAMOSA project is both ambitious by the extent and variety of analyses that will be made and innovative since it proposes to build a gene regulation network not limited to a 'model strain', but including ecotypic variability, an important step towards the development of a 'model genus'. We aim at constructing a gene network model sufficiently flexible to allow the integration of forthcoming transcriptomic and physiological data. Many results should be extendable to other ecosystems, since relatives of these microorganisms are found in virtually all illuminated aquatic environments including rivers, lakes, hotsprings, etc. Other outcomes include a better appraisal of the ecosystemic and industry-related services potentially offered by these marine cyanobacteria, and hence will be useful for durable management and valorization of marine ecosystems in which these microorganisms constitute a significant and potentially exploitable component.