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Do Synechococcus regulatory networks underpin marine ecological distinctness?

Final Report Summary - SYNERGY (Do Synechococcus regulatory networks underpin marine ecological distinctness?)

“SYNERGY”

Do Synechococcus regulatory networks underpin marine ecological distinctness?

Anthropogenic effects on global biogeochemical cycles have been, in part, buffered by the vast marine ecosystem, with bacteria playing a key role in this process. Of particular importance is the structure of bacterial populations because the large-scale processes of ecosystems depend on the principal constituent of communities and organisms therein. More fundamentally, defining the structure of microbial populations has implications for bacterial species definition as well as questions regarding the ecological importance of genotypic variation. Indeed, knowledge of the latter and the factors that dictate global community structure are vital to predict future large-scale climatic changes.

Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic organisms in marine ecosystems and, therefore, on Earth. They are considered among the major primary producers in oceanic waters. Members of the Synechococcus genus are ubiquitous, with colonisation of the marine ecosystem facilitated by specific adaptations to cope with gradients of nutrients and light quality. As well as daily and seasonal patterns in the solar light environment, there can also be associated changes in water column structure delineating stratified versus well-mixed water columns. These factors allow for the occurrence of generalists (or opportunists) which are present throughout the year and capable of responding to a wide spectrum of environmental change, and specialists which are restricted to a specific niche in space or time. Comparative genomics of the different sequenced Synechococcus species by the Scanlan group has shown that shared gene content is consistent with phylogeny and the broad ‘generalist’ and ‘opportunist’ lifestyle strategies mentioned above.

This project has focused on elucidating whether the distinctive genomic regulation potential is consistent with niche colonization, using iron starvation stress as a case study. Interestingly, the coastal opportunist strain Synechococcus sp. CC9311 showed a strong genetic regulation under iron depletion by increasing transport systems and decreasing the intracellular demand for this metal. On the other hand, the other strains Synechococcus sp. BL107 (an open-ocean mesotroph), Synechococcus sp. WH8102 (an open-ocean oligotroph) and Synechococcus sp. WH7803 (an open-ocean opportunist) did not show such a strong regulatory network. This would be consistent with the fact these three open-ocean strains are adapted to a chronic iron depletion and adaptation to this stress is almost constitutive. Even so, and most interestingly, was the observation that a significant number of up and down-regulated genes observed during the response to iron depletion stress were encoded within genomic islands. This seems to be a trend observed in many different kinds of stresses applied to Synechococcus and highlights how niche adaptation of different bacterial ecotypes has been acquired by horizontal gene transfer only after strain differentiation.

The project also developed an initially unforseen angle to understand how Synechococcus strains interacted with naturally co-occurring heterotrophic strains and how they establish mutualistic exchange of functions within a niche. It is known that healthy, well-balanced ecosystems are made up of multiple interacting food chains. In marine systems, like all ecosystems, organisms obtain carbon and energy from more than one source, and may have several predators. In surface seawater (as for most of the water column), photosynthetic primary producers or phytoplankton are the main source of carbon and energy that sustain the whole ecosystem despite their relatively low numerical abundance and contribution to biomass (under 10% of total plankton). Phytoplankton, due to leakage, inefficient grazing or viral lysis, can release large amounts of dissolved and particulate organic matter (DOM and POM) that can then be used by the numerous existing heterotrophic microorganisms present in the water column. Heterotrophs will re-mineralise most of this organic matter recycling essential elements i.e. nitrogen, phosphorus and trace-metals, within this nutrient-poor ecosystem. The physiology of co-cultures between Synechococcus (photoautotroph) and Roseobacter (heterotroph) showed these were much more robust and had longer survival periods than Synechococcus cultures grown axenically. Proteomic analysis of cellular and extracellular fractions of these cultures showed how the heterotroph expresses a large number of transporters and catalytic exoenzymes in order to remove the organic matter generated by the phototroph, which otherwise would continue to accumulate in the milieu until toxic concentrations were reached. The differentially expressed genes in Synechococcus were mostly of unknown function highlighting the dearth of knowledge we currently have on microbial interactions and in which Dr Christie-Oleza will continue to develop his scientific career.

These findings, together with the difficulty of reliable genetic manipulation of Synechococcus via homologous recombination led Dr Christie-Oleza to develop a new methodology during the tenure of this fellowship. In this sense, genetic manipulation in Synechococcus is feasible when a “helper” strain (in this case the Roseobacter heterotroph) is present in order to “decontaminate” the media from dead sensitive non-mutant cells that otherwise generate toxic debris to the genetically-manipulated Synechococcus strain. The Roseobacter strain can then be counter-selected in order to re-establish the axenic strain of the photoautotroph.

All findings, results, discussion and conclusions generated during the tenure of this IEF Marie Curie fellowship “Synergy” will be shortly made available to the scientific community in the form of relevant scientific publications.