Extremely reduced supergroup F Wolbachia: transition to obligate insect symbionts

Abstract

Wolbachia are widely distributed symbionts among invertebrates that manifest by a broad spectrum of lifestyles from parasitism to mutualism. Wolbachia Supergroup F is considered a particularly interesting group which gave rise to symbionts of both arthropods and nematodes, and some of its members are obligate mutualists. Further investigations on evolutionary transitions in symbiosis have been hampered by a lack of genomic data for Supergroup F members. In this study, we present genomic data for five new supergroup F Wolbachia strains associated with four chewing lice species. These new strains in different evolutionary stages show genomic characteristics well-illustrating the evolutionary trajectory which symbiotic bacteria experience during their transition to mutualism. Three of the strains have not yet progressed with the transition, the other two show typical signs of ongoing gene deactivation and removal (genome size, coding density, low number of pseudogenes). Particularly, wMeur1, a symbiont fixed in all Menacanthus eurystenus populations across four continents, possesses a highly reduced genome of 733,850 bp with a horizontally acquired capacity for pantothenate synthesis. Comparing with other strains showed wMeur1 genome as the smallest currently known among all Wolbachia and the first example of Wolbachia which has completed genomic streamlining known from the gammaproteobacterial obligate symbionts.

A highly divergent Wolbachia with a tiny genome in an insect-parasitic tylenchid nematode

“…While the genomes of facultative Wolbachia symbionts of arthropods, such as strains that cause cytoplasmic incompatibility, lie in the range of approximately 1–1.5 Mb, genomes of obligate Wolbachia symbionts of filarial nematodes are smaller, ranging from 860 kb to approximately 1.1 Mb. Up to now, the smallest reported Wolbachia genome, described in a recent preprint, is that of a symbiont of Menacanthus chewing lice, within Wolbachia supergroup F, a group that includes symbionts of other blood-feeding insects and some filarial nematodes, at approximately 733 kbp [ 55 ]. Another common feature of obligate symbionts is loss of genes involved in DNA replication, repair and recombination, which is thought to drive incredibly rapid rates of substitution [ 39 , 56 , 57 ].…”

“…Despite being so highly divergent, the w How genome is a complete subset of all other Wolbachia , unlike the reduced genome Wolbachia in Menacanthus chewing lice, for example, which has horizontally acquired genes involved in panthotenate synthesis [ 55 ]. Interestingly, while w How has lost a huge number of genes, it has retained some, but not all, pathways that are also found in filarial nematode symbionts, which have been independently colonized at least three times by different lineages of Wolbachia [ 25 ], all of which have converged on a similar complement of genes.…”

Phylogenomic analysis of Wolbachia genomes from the Darwin Tree of Life biodiversity genomics project

“…As expected, supergroups that were not well represented often contained more strain-specific genes. For example, wCfeT from supergroup E (which infects cat fleas, Ctenocephalides felis ) uniquely encoded genes for pantothenate (panC-panG-panD-panB) [ 36 ] and thiamine (thiG-thiC) biosynthesis. Nonetheless, out of the ten genomes with most strain-specific genes, seven belonged to either supergroup A or B.…”

An endosymbiont harvest: Phylogenomic analysis of Wolbachia genomes from the Darwin Tree of Life biodiversity genomics project

“…As expected, supergroups which were not well represented often contained more strain-specific genes. For example, wCfeT from supergroup E (which infects cat fleas, Ctenocephalides felis ) uniquely encoded genes for pantothenate (panC-panG-panD-panB) 32 and thiamine (thiG-thiC) biosynthesis. Nonetheless, out of the ten genomes with most strain-specific genes, seven belonged to either supergroup A or B.…”