Diversity and evolution of surface polysaccharide synthesis loci in Enterobacteriales

Abstract

Bacterial capsules and lipopolysaccharides are diverse surface polysaccharides (SPs) that serve as the frontline for interactions with the outside world. While SPs can evolve rapidly, their diversity and evolutionary dynamics across different taxonomic scales has not been investigated in detail. Here, we focused on the bacterial order Enterobacteriales (including the medically relevant Enterobacteriaceae), to carry out comparative genomics of two SP locus synthesis regions, cps and kps, using 27,334 genomes from 45 genera. We identified high-quality cps loci in 22 genera and kps in 11 genera, around 4% of which were detected in multiple species. We found SP loci to be highly dynamic genetic entities: their evolution was driven by high rates of horizontal gene transfer (HGT), both of whole loci and component genes, and relaxed purifying selection, yielding large repertoires of SP diversity. In spite of that, we found the presence of (near-)identical locus structures in distant taxonomic backgrounds that could not be explained by recent exchange, pointing to long-term selective preservation of locus structures in some populations. Our results reveal differences in evolutionary dynamics driving SP diversity within different bacterial species, with lineages of Escherichia coli, Enterobacter hormaechei and Klebsiella aerogenes most likely to share SP loci via recent exchange; and lineages of Salmonella enterica, Citrobacter sakazakii and Serratia marcescens most likely to share SP loci via other mechanisms such as long-term preservation. Overall, the evolution of SP loci in Enterobacteriales is driven by a range of evolutionary forces and their dynamics and relative importance varies between different species.

Long read metagenomics, the next step?

“…Furthermore, many key ecological functions such as transporters, degradation of resilient compounds, virulence factors and many others are also found in these genomic regions [78,79]. That the long replacement GI4 do not assemble in the MED4 LRa MAG was to be expected given the high diversity of very polyclonal microbes such as Prochlorococcus [80] and the length of this specific fGI involved in the synthesis of the O-chain polysaccharide [81,82]. The presence of multiple (and long) versions of GI4 might disorient the assembler that has many possibilities to continue the contig.…”

Genomic diversity and organization of complex polysaccharide biosynthesis clusters in the genus Dickeya

“…A recent study shows that genetic exchanges in bacteria encoding capsules are frequent and lead to changes in genome dynamics [46,57]. Variation at the LPS biosynthesis cluster in phytopathogenic Gram-negative bacteria, Xanthomonas oryzae pv.…”

Nutrient conditions are primary drivers of bacterial capsule maintenance in Klebsiella

“…In Klebsiella pneumoniae, there are at least 77 serologically defined capsule serotypes [ 15 , 16 ], and more than 130 serotypes identified through comparative genomics [ 17 , 18 ]. This serotype diversity results from the faster evolution of capsular loci compared to that of the rest of the genome owing to high rates of homologous recombination [ 19 , 20 ], and horizontal gene transfer [ 21 , 22 ]. As a result, the same capsular serotype can be found in multiple lineages of K. pneumoniae and a monophyletic clade can include distinct serotypes [ 20 ].…”