Marine Bacteroidetes: Distribution patterns and role in degradation of organic matter

Abstract

Oceans occupy two thirds of the Earth's surface, have a key role in biogeochemical cycles, and hold a vast biodiversity. Microorganisms in the world oceans are extremely abundant, their abundance is estimated to be 1029. They have a central role in the recycling of organic matter, therefore they influence the air-sea exchange of carbon dioxide, carbon flux through the food web, and carbon sedimentation by sinking of dead material. Bacteroidetes is one of the most abundant bacterial phyla in marine systems and its members are hypothesized to play a pivotal role in the recycling of organic matter. However, most of the evidence about their role is derived from cultivated species. Bacteroidetes is a highly diverse phylum and cultured strains represent the minority of the marine bacteroidetal community, hence, our knowledge about their ecological role is largely incomplete. In this thesis Bacteroidetes in open ocean and in coastal seas were investigated by a suite of molecular methods. The diversity and clade-specific abundance of Bacteroidetes were analyzed in different oceanic provinces in the North Atlantic Ocean. Comparative sequence analysis of 16S ribosomal RNA (rRNA) gene libraries revealed a high diversity and significant spatial variability. Major bacteroidetal clades were delimited based on 16S rRNA gene sequence identities and further quantified by fluorescence in situ hybridization (FISH). Preliminary FISHanalysis indicated that certain Bacteroidetes clades were present in numbers lower than the detection limit of the method. Therefore, the FISH quantification protocol was modified by increasing the sample volume, which allowed us to reliably quantify populations down to absolute numbers of only 500 cells ml-1.All bacteroidetal clades evaluated showed pronounced regional distribution patterns. Interestingly, our analysis revealed that the bacteroidetal community composition largely reflects the satellite space-based demarcation of ocean provinces. Large insert fosmid-based metagenomic libraries constructed from two distinct oceanic provinces in the North Atlantic Ocean and an extensive genome comparison gave first insights into an adaptation of the bacteroidetal community to distinct environmental conditions. Genomic analysis highlighted that marine Bacteroidetes have a marked metabolic potential for the degradation of proteins and bacterial cell wall components, particularly in oligotrophic water masses. Our findings also provide evidence of a strong specialization for the degradation of particular polymers. Glycolytic potential was confined to a member of the genus Polaribacter which had several glycoside hydrolases, and a higher number of sulfatases than other members of the same genus. This Polaribacter flavobacterium might represent an ecotype within the genus with a particular adaptation for the degradation of sulfated polysaccharides, known to be major constituents of phytoplankton cell walls. Supporting the hypothesis of Bacteroidetes as particle inhabitants, a specific in situ enrichment of certain bacteroidetal clades in the phycosphere of phytoplankton cells was proved in the phytoplankton-rich oceanic province. We could establish a link between Bacteroidetes metabolic information, organism identity, and abundance, thus providing hints with respect to the significance of certain metabolic traits. Furthermore, the Bacteroidetes clades delimited in the open ocean were also identified in the coastal systems analyzed in this thesis, giving evidence about the ecological relevance of those bacteroidetal clades in different marine settings. In summary, the combination of genomics and diversity studies allowed us to link main aspects about the Bacteroidetes community, enabling the better understanding of their ecological role in marine systems.