Geographic Genetic Divergence in Tychoplanktonic Taxa Dominating Diatom Communities in Marine Biofilms

Abstract

Diatoms constitute the main photosynthetic group in marine biofilms throughout the world's oceans, in particular, on plastic debris, which has become a major problem in the marine environment. However, they remain largely unexplored in this context compared to prokaryotes. Here, we aim to understand the dynamics of diatom communities in the plastisphere at different levels: how taxa are selected from the planktonic community and how communities are structured over time and at large spatial scales. Biofilms were collected from PVC (polyvinyl chloride) panels immersed (i) for 1 year in two NW Mediterranean sites, a mesotrophic one (Toulon Bay) and an oligotrophic one (Banyuls Bay), and (ii) for 1 month in Toulon Bay and two other eutrophic sites (Lorient in South Brittany in the Atlantic Ocean and Reunion Island in the Indian Ocean). Plastispheres were analyzed using both microscopic and molecular approaches, focusing on the relationship between diatoms and other microorganisms in biofilms. Light microscopy revealed spatio-temporal differences in cell abundance and biovolume. Metabarcoding, targeting the rbcL gene for diversity and composition, revealed that the richness of diatom species was already maximal in the early stages of biofilm formation, and beta-diversity showed a clear temporal evolution in the Mediterranean Sea. Including prokaryotic and fungal communities, we described microorganism interactions within biofilms throughout the colonization process of the plastisphere. In addition, environmental parameters on a large geographical scale were shown to be stronger drivers in structuring diatom communities, considering both planktonic and biofilm lifestyles. A core biofilm community represented by a few abundant species was observed across sites. The occurrence of tychoplanktonic taxa emphasizes the specificity of diatoms among other microorganisms in biofilms. Finally, the complete absence of common genetic variants among Lorient, Reunion Island, and Toulon suggests that dispersal by marine currents over a large geographical scale has led to adaptation processes.