Evolutionary Genomics of an Ancient Prophage of the Order Sphingomonadales

Abstract

The order Sphingomonadales, containing the families Erythrobacteraceae and Sphingomonadaceae, is a relatively less well-studied phylogenetic branch within the class Alphaproteobacteria. Prophage elements are present in most bacterial genomes and are important determinants of adaptive evolution. An “intact” prophage was predicted within the genome of Sphingomonas hengshuiensis strain WHSC-8 and was designated Prophage IWHSC-8. Loci homologous to the region containing the first 22 open reading frames (ORFs) of Prophage IWHSC-8 were discovered among the genomes of numerous Sphingomonadales. In 17 genomes, the homologous loci were co-located with an ORF encoding a putative superoxide dismutase. Several other lines of molecular evidence implied that these homologous loci represent an ancient temperate bacteriophage integration, and this horizontal transfer event pre-dated niche-based speciation within the order Sphingomonadales. The “stabilization” of prophages in the genomes of their hosts is an indicator of “fitness” conferred by these elements and natural selection. Among the various ORFs predicted within the conserved prophages, an ORF encoding a putative proline-rich outer membrane protein A was consistently present among the genomes of many Sphingomonadales. Furthermore, the conserved prophages in six Sphingomonas sp. contained an ORF encoding a putative spermidine synthase. It is possible that one or more of these ORFs bestow selective fitness, and thus the prophages continue to be vertically transferred within the host strains. Although conserved prophages have been identified previously among closely related genera and species, this is the first systematic and detailed description of orthologous prophages at the level of an order that contains two diverse families and many pigmented species.

Machine-Learning Classification Suggests That Many Alphaproteobacterial Prophages May Instead Be Gene Transfer Agents

“…Genes in the detected RcGTA-like head–tail clusters remain mainly unannotated as “gene transfer agents” in GenBank records, and therefore they can be easily confused with prophages. For example, recently described “conserved prophage” in Sphingomonadales (Viswanathan et al. 2017) is predicted to be an RcGTA-like element by GTA-Hunter.…”

Host selection tendency of key microbiota in arid desert lichen crusts

“…So we speculated that these bacteria existing in lichen strata might not be occasional. Besides, the acquisition of sunlight was limited in R as underground stratum, the abundant Sphingomonadales here indicates a possible pathway because Sphingomonadales consist of aerobic anoxygenic phototrophs with diverse carotenoid pigments and photosynthesis gene clusters (PGCs) [ 60 , 61 ]. The source of nitrogen acquisition in chlorolichens such as Endocarpon is not completely clear, therefore, the abundance of Rhizobiales in L attracted our attention, which was also found to be common in other chlorolichens, [ 12 ] however, there is no evidence to support Rhizobiales help in nitrogen fixation in the chlorolichens like in the plants [ 57 ].…”

Phylogenetic insights into the diversity of Chryseobacterium species

“…Phylogenetic analysis using the web server CVTree3, which is an alignment- and parameter-free method that relies on the oligopeptide content (K-tuple length) of conserved proteins to deduce evolutionary relatedness [ 12 ], was performed as described previously [ 13 ].…”