Large diversity in the O-chain biosynthetic cluster within populations of Pelagibacterales

Abstract

ABSTRACTWe have used single-amplified genomes (SAGs) and long-read metagenomics to examine the diversity of the O-chain polysaccharide biosynthesis cluster (OBC) in marine bacteria of the Pelagibacterales order. OBCs are notorious for their diversity and have been used to type strains in pathogens and saprophytes, but their patterns of variation in free-living bacteria are little known. We found that, for these marine heterotrophic bacteria, the diversity is comparable to that of saprophytes, such as Enterobacteriales i.e. nearly each strain carries a different OBC. However, although OBC inheritance was largely vertical, the existence of some shared clusters allowed a comparative analysis. The OBCs diverge along with the genome, which is taken as indicative of old horizontal gene transfer (HGT) events. Only 14 cases of recent HGT were detected and they happened independently of taxonomy or location. Thus, although the O-chain is a major phage receptor in Gram-negative bacteria, the exchange of the complete cluster seems to play a minor role in the phage-bacterium arms-race. By long-read metagenomics, we could detect 380 different OBCs in a single sampling site in the Mediterranean. A single population (single species and sample) of the endemic Ia.3/VII genomospecies had a set of 158 OBCs of which 130 were different. This large diversity in clonal lineages might reflect the large amount of metabolic pathways required to deal with the enormous chemical diversity of dissolved organic matter in the ocean.