Diminutive, degraded but dissimilar: Wolbachia genomes from filarial nematodes do not conform to a single paradigm

Abstract

Wolbachia are alpha-proteobacteria symbionts infecting a large range of arthropod species and two different families of nematodes. Interestingly, these endosymbionts are able to induce diverse phenotypes in their hosts: they are reproductive parasites within many arthropods, nutritional mutualists within some insects and obligate mutualists within their filarial nematode hosts. Defining Wolbachia ‘species’ is controversial and so they are commonly classified into 17 different phylogenetic lineages, termed supergroups, named A–F, H–Q and S. However, available genomic data remain limited and not representative of the full Wolbachia diversity; indeed, of the 24 complete genomes and 55 draft genomes of Wolbachia available to date, 84 % belong to supergroups A and B, exclusively composed of Wolbachia from arthropods. For the current study, we took advantage of a recently developed DNA-enrichment method to produce four complete genomes and two draft genomes of Wolbachia from filarial nematodes. Two complete genomes, wCtub and wDcau, are the smallest Wolbachia genomes sequenced to date (863 988 bp and 863 427 bp, respectively), as well as the first genomes representing supergroup J. These genomes confirm the validity of this supergroup, a controversial clade due to weaknesses of the multilocus sequence typing approach. We also produced the first draft Wolbachia genome from a supergroup F filarial nematode representative (wMhie), two genomes from supergroup D (wLsig and wLbra) and the complete genome of wDimm from supergroup C. Our new data confirm the paradigm of smaller Wolbachia genomes from filarial nematodes containing low levels of transposable elements and the absence of intact bacteriophage sequences, unlike many Wolbachia from arthropods, where both are more abundant. However, we observe differences among the Wolbachia genomes from filarial nematodes: no global co-evolutionary pattern, strong synteny between supergroup C and supergroup J Wolbachia, and more transposable elements observed in supergroup D Wolbachia compared to the other supergroups. Metabolic pathway analysis indicates several highly conserved pathways (haem and nucleotide biosynthesis, for example) as opposed to more variable pathways, such as vitamin B biosynthesis, which might be specific to certain host–symbiont associations. Overall, there appears to be no single Wolbachia –filarial nematode pattern of co-evolution or symbiotic relationship.

Extremely reduced supergroup F Wolbachia: transition to obligate insect symbionts

“…When assessed against Rickettsiales database, the average completeness was 95% (85.7%-98.7%). The assessment against Proteobacteria, performed to provide direct comparison with Lefoulon et al (10), produced considerably lower average of 78.9% (68.5%-83.5%) corresponding to the results of Lefoulon et al (10). For the wAlce strain, Busco predicted a higher degree of possible duplications, indicating that this assembly may not contain a single Wolbachia strain but could rather be a mixture of two closely related strains.…”

“…Assessment of metabolic capacities was done using the web-based tools Blastkoala and KEEG mapper (57). To obtain a metabolic overview comparable with other Wolbachia supergroups, we adopted the scheme used by Lefoulon et al (10) and extended its content with comparison of amino acids synthesis.…”

“…Occasional screenings suggest that the supergroups underrepresented by genomic data may encompass a high diversity of Wolbachia strains. As an example, supergroup F, currently represented by four genomes and genome drafts from two nematodes and two arthropods (1,(8)(9)(10), seems to contain a wide variety of Wolbachia from different hosts when screened for specific Wolbachia genes (2,(11)(12)(13).…”

Growth and Maintenance of Wolbachia in Insect Cell Lines

“…As more strains are described, nomenclature based on species names of hosts is becoming cumbersome. For example, wCtub could refer to a supergroup J Wolbachia from a filarial worm [26] or a supergroup F Wolbachia from a termite [27].…”

Molecular detection of Wolbachia endosymbiont in reptiles and their ectoparasites

“…Meanwhile, arthropod- Wolbachia association could be considered more parasitic, since the bacteria gain fitness advantage by reproductive manipulations of the host, modifying the iron homeostasis and reducing the vector capacity of their hosts (Bandi et al 2001 ; Kremer et al 2009 ; Martinez et al 2017 ). Based on their genetic evolution, Wolbachia have been classified as 17 supergroups, from A to S (Fenn et al 2006 ; Lefoulon et al 2020a , b ), in which Wolbachia of arthropods were included in supergroups A, B, E, H, I, K, that of nematodes in C, D, J (Glowska et al 2015 ) and plant-parasitic nematodes in L (Brown et al 2016 ). Among these supergroups, F is an exception being reported in both arthropods (i.e.…”