Highly clade-specific biosynthesis of rhamnose: present in all plants and in only 42% of prokaryotes. OnlyPseudomonasuses both D- and L-rhamnose

Abstract

ABSTRACTRhamnose is a constituent of lipo- and capsular polysaccharides, and cell surface glycoproteins. L-rhamnose is biosynthesized by the rml or udp pathway and D-rhamnose by the gdp pathway. Disruption of its biosynthesis affects survival, colonisation, etc. Rhamnosides are commercially important in pharmaceutical and cosmetics industries. HMM profiles were used to investigate the prevalence of the three pathways in completely sequenced genomes and metagenomes. The three pathways are mutually exclusive except inPseudomonaswhich has both rml and gdp pathways. The rml pathway is restricted to bacteria (42% genomes), archaea (21%) and bacteriophages, and absent in eukaryotes and other viruses. The gdp pathway is restricted toPseudomonasandAneurinibacillus. The udp pathway is primarily found in plants, fungi and algae, and in human faecal metagenomic samples. The rml pathway is found in >40% genomes of Actinobacteria, Bacteroidetes, Crenarchaeota, Cyanobacteria, Fusobacteria and Proteobacteria but in <20% genomes of Chlamydiae, Euryarchaeota and Tenericutes. The udp pathway is found in all genomes of Streptophyta, <=25% genomes of Ascomycota and Chordata, and none of the genomes of Arthropoda and Basidiomycota. Some genera which lack any of these pathways areChlamydia,Helicobacter,Listeria,Mycoplasma,Pasteurella,RickettsiaandStaphylococcus. Organisms such asE. coliandSalmonella entericashowed significant strain-specific differences in the presence/absence of rhamnose pathways. Identification of rhamnose biosynthesis genes facilitates profiling their expression pattern, and in turn, better understanding the physiological role of rhamnose. Knowledge of phylogenetic distribution of biosynthesis pathways helps in fine graining the taxonomic profiling of metagenomes.AUTHOR SUMMARYIn the present study, we have investigated the prevalence of rhamnose biosynthesis pathways in completely sequenced genomes and metagenomes. It is observed that the prevalence of rhamnose is highly clade specific: present in all plants but in less than half of all prokaryotes. Among chordates, only the Chinese rufous horseshoe bat has rhamnose biosynthesis pathway and this exclusive presence is quite baffling. The effect of disrupting rhamnose biosynthesis has been reported in a few prokaryotes and all these cases pointed to the essentiality of rhamnose for critical physiological processes such as survival, colonisation, etc. In this background, it is surprising that many of the prokaryotes such asEscherichia coliandSalmonella entericashow significant strain-specific differences in the presence/absence of rhamnose pathway. This study will facilitate the experimental characterization of rhamnose biosynthesis genes in organisms where this pathway has not been characterised yet, eventually leading to the elucidation of the biological role of rhamnose. Phylum-, genus-, species- and strain-level differences found with respect to presence of rhamnose biosynthesis pathway genes can be used as a tool for taxonomic profiling of metagenome samples. This study could also annotate a significant number of orphan proteins in the TrEMBL database.