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Molecular Drivers of the InteractionS between marine algicidal KORdia and DIAtoms: from coexistence to algal lysis.

Periodic Reporting for period 1 - DISKORDIA (Molecular Drivers of the InteractionS between marine algicidal KORdia and DIAtoms: from coexistence to algal lysis.)

Okres sprawozdawczy: 2022-07-01 do 2024-01-31

Marine microorganisms such as phytoplankton and bacteria play essential roles that shape the world we live in. Through photosynthesis, marine phytoplankton convert inorganic carbon into organic matter that fuels marine food webs. Marine bacteria recycle at least half of the organic matter produced by phytoplankton, which makes important nutrients and vitamins available again for phytoplankton. In addition to sustaining life in the ocean, the activity of these microorganisms impacts the concentration of carbon in the Earth’s atmosphere, which in turns affects climate. Thus, phytoplankton and bacteria need each other to thrive and perform these important functions that set the conditions for life on Earth.
In the 1970s, marine microbiologists discovered unusual bacteria that behave like phytoplankton pathogens, inhibiting photosynthesis and growth, and sometimes even inducing death and cell lysis. To date, very little is known about these so-called algicidal bacteria, and important questions remain about their mechanisms of attack and the consequences of their behavior for phytoplankton physiology and activity. The DISKORDIA project was designed to shed light on several aspects of the biology of these algicidal bacteria through the study of Kordia, a genus of marine algicidal bacteria.
The first discovered member of the Kordia genus, Kordia algicida, was isolated from seawater in the Masan Bay (Republic of Korea) and showed algicidal behaviour against local species of phytoplankton. Since the isolation of K. algicida, nine other Kordia isolates have been obtained from multiple oceanic regions, suggesting this bacterial group is ubiquitously distributed in the world ocean. The objective of the DISKORDIA project was to investigate the mechanisms of algicidal activity in Kordia bacteria and provide answers to the following questions:
-are all Kordia species capable of algicidal activity?
-what is the sensitive phytoplankton spectrum for algicidal Kordia species?
-what is the effect of algicidal Kordia on sensitive phytoplankton?
-what is the algicidal mechanism of Kordia species and is it the same among all of them?
Answering these questions is essential to understand how they affect phytoplankton physiology and diversity and thus predict the impact of algicidal bacteria in marine systems.
Lab experiments were performed to investigate algicidal activity in the 10 species of Kordia marine bacteria available in culture. Co-cultures of each Kordia strain with 54 distinct phytoplankton strains representing a large range of taxa (diatoms, dinoflagellates, chlorophytes, raphidophytes, haptophytes, and cyanobacteria) showed that all Kordia species are algicidal against at least 3 phytoplankton strains. Interestingly, the number and identity of sensitive phytoplankton strains differed among Kordia species and revealed that 6 of the 10 species had a broad spectrum of sensitive phytoplankton strains (between 18 and 31) while the 4 remaining Kordia affected a smaller range of phytoplankton strains (between 3 and 12). At least one strain from each phytoplankton taxa tested was sensitive to at least one Kordia species. These results show that overall, the Kordia genus is capable of negatively impacting a wide spectrum of phytoplankton taxa.
Further experiments were performed to decipher the mechanism of the algicidal attack. Co-cultures of a sensitive diatom strain with each of the 10 Kordia species showed conserved effects of the different Kordia on the diatom. These experiments showed a quick inhibition of the diatom growth followed by rapid depletion of the diatom chlorophyll content. Changes in diatom chlorophyll content were accompanied by decreased photosynthetic efficiency. These effects were also observed in the presence of Kordia culture filtrates instead of the Kordia themselves, demonstrating that the attack is mediated by extracellular release of one or several algicidal molecule(s). Interestingly, membrane integrity markers showed that no changes in the integrity of the diatom membrane were observed in these experiments, suggesting that, instead of cell lysis, a yet elusive mechanism is involved in chlorophyll a depletion. Finally, experiments where different Kordia preculture conditions were tested showed that no activation of the bacteria by phytoplankton cues were necessary to trigger the attack, but that Kordia growth rather than abundances was necessary to observe an efficient bacterial attack.
Overall, the results of this project suggest that, despite large genetic differences between the 10 Kordia species, a common algicidal mechanism involving the production of extracellular compounds that inhibit phytoplankton growth and photosynthesis and trigger chlorophyll depletion in otherwise intact phytoplankton cells is conserved in this marine bacterial genus. The ongoing analysis of Kordia genome expression during phytoplankton attack will further pinpoint the biosynthetic pathways involved in Kordia algicidal activity. Through these conserved algicidal features, the Kordia group can attack a large range of phytoplankton taxa, making this ubiquitous marine bacterial genus an excellent model to study the conditions and ecological consequences of bacterial algicidal activity in the ocean in subsequent research projects.
The results from this project raise many new questions about the role of algicidal bacteria in marine ecosystems, that will fuel new research projects. For instance, an unexpected result from the DISKORDIA project is the observation of reduced or even suppressed algicidal effects of Kordia bacteria on otherwise sensitive phytoplankton in the presence of other bacteria. These observations suggest that other microbial interactions such as substrate competition or antagonism among bacteria play an important role in the growth and activity of algicidal bacteria. The project Coordinator has obtained a permanent position as a CNRS researcher in France and will continue to investigate the physiology, ecology, and biogeochemical implications of algicidal activity in marine bacteria, building on the results from the DISKORDIA project.
Diatom cultures alone (top) or with algicidal Kordia bacteria (bottom)
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