Genomic Analysis of Wolbachia from Laodelphax striatellus (Delphacidae, Hemiptera) Reveals Insights into Its “Jekyll and Hyde” Mode of Infection Pattern

Abstract

Wolbachia is a widely distributed intracellular bacterial endosymbiont among invertebrates. The wStriCN, the Wolbachia strain that naturally infects an agricultural pest Laodelphax striatellus, has a “Jekyll and Hyde” mode of infection pattern with positive and negative effects: It not only kills many offspring by inducing cytoplasmic incompatibility (CI) but also significantly increases host fecundity. In this study, we assembled the draft genome of wStriCN and compared it with other Wolbachia genomes to look for clues to its Jekyll and Hyde characteristics. The assembled wStriCN draft genome is 1.79 Mb in size, which is the largest Wolbachia genome in supergroup B. Phylogenomic analysis showed that wStriCN is closest to Wolbachia from Asian citrus psyllid Diaphorina citri. These strains formed a monophylogentic clade within supergroup B. Compared with other Wolbachia genomes, wStriCN contains the most diverse insertion sequence families, the largest amount of prophage sequences, and the most ankyrin domain protein coding genes. The wStriCN genome encodes components of multiple secretion systems, including Types I, II, IV, VI, Sec, and Tac. We detected three pairs of homologs for CI factors CifA and CifB. These proteins harbor the catalytic domains responsible for CI phenotypes but are phylogenetically and structurally distinct from all known Cif proteins. The genome retains pathways for synthesizing biotin and riboflavin, which may explain the beneficial roles of wStriCN in its host planthoppers, which feed on nutrient-poor plant sap. Altogether, the genomic sequencing of wStriCN provides insight into understanding the phylogeny and biology of Wolbachia.

The Biochemistry of Cytoplasmic Incompatibility Caused by Endosymbiotic Bacteria

“…Sequence analysis of various CI-inducing Wolbachia strains subsequently showed that the cidA-cidB-related syntenic genes fall into one of five distinct phylogenetic clades (Types I to V) [25,35,36]. In several examples, these coupled genes are expressed as bicistronic mRNAs [34,37].…”

“…In the alternative phylogenic classification scheme, Type I Cifs are equivalent to Cids, while types II-IV are all cin operon variants. Interestingly, several of the Type V operons encode B proteins predicted to have both active nuclease and DUB domains [36,40].…”

“…Interestingly, in most-but not all-CI-inducing Wolbachia strains, the Cifs are found as part of a "eukaryotic association module" (EAM) within a viral prophage [36,46]. The link to these WO prophages may reflect how the EAM genes, including those responsible for CI, were acquired by different Wolbachia strains; active WO phage particles can be generated from these prophages, a potential means of horizontal gene transfer and possibly even vertical transmission [47].…”

Evolution-guided mutagenesis of the cytoplasmic incompatibility proteins: Identifying CifA’s complex functional repertoire and new essential regions in CifB

“…Finally, STE domains mediate 96 transcriptional induction in yeast (Wong Sak Hoi and Dumas, 2010). Structural homology 97 predictions identify the STE and Puf-family RNA-binding domains across four and five 98 phylogenetic Cif Types respectively, whereas the catalase-rel domain is only annotated in Type 99 1 (Bing et al, 2020;Lindsey et al, 2018). 100…”

“…Mutation of conserved sites within the STE had no impact on either CI or rescue. This was 427 surprising since the STE domain appeared structurally conserved across four of the five CifA 428 phylogenetic Types(Bing et al, 2020;Lindsey et al, 2018). However, while the sites mutated in 429 the domain were conserved, the remainder of the domain appears to evolving mostly neutrally 430(Shropshire et al, 2018), suggesting the domain may be of lesser importance than N-terminal 431 regions.…”