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

Abstract

In this study, we have used single-amplified genomes (SAGs) and long-read metagenomics to examine the intrapopulation 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 major photoheterotrophic bacteria, the diversity is comparable to that of saprophytes, such as Enterobacteriales i.e. nearly each strain carries a different OBC involved in its synthesis. Therefore, different OBCs had completely different gene complements, as they had few ortholog genes. However, although OBC inheritance was largely vertical, the existence of some shared clusters allowed a comparative analysis that showed that the cluster diverges along with the genome, indicative of old horizontal gene transfer (HGT). Only 14 cases of recent HGT were detected and they happened independently of taxonomy or location. 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 arms-race evolution. However, dN/dS was significantly larger for the genes in the OBC than for the whole genome so OBC genes appear to be more variable. 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.

Contrasting defense strategies of oligotrophs and copiotrophs revealed by single-cell-resolved virus–host pairing of freshwater bacteria

“…Indeed, a pangenome graph of our Pelagibacteraceae SAGs demonstrated that their HVR2 regions were nearly unique to individual cells (Fig. S10), as also reported in a recent study of marine Pelagibacteraceae (71). Unlike the fluctuating abundance of copiotrophs, oligotrophs are less likely to be affected by population bottlenecks and thus maintain their genetic microdiversity (7).…”

Microdiversity in marine pelagic ammonia-oxidizing archaeal populations

“…However, the most common version of this fGI (36 LRs) was not similar to the one of the Pacific Ocean isolate, with a deletion of most of the ORFs present in the SPOT01 genomic island (94%) (Figure 2B, lower part). Either for N. brevis or for N. catalinensis, the diversity of sequence of the glycosylation fGIs was much lower than that found in other microbes (Coleman et al 2006; Haro-Moreno et al 2024). However, in both cases, there seems to be decreased synteny towards the center of the island.…”

“…In a recent study, some of us have studied the diversity of O-chain polysaccharide genomic islands in Pelagibacterales (heterotrophic bacteria) and have found a very large diversity, reaching easily 130 different gene clusters in a single population (single species single sample) (Haro-Moreno et al, 2024). This is in sharp contrast to the results described here for a chemolithotrophic archaeon.…”