Diminutive, degraded but dissimilar:Wolbachiagenomes from filarial nematodes do not conform to a single paradigm
Authors: Lefoulon Emilie , Clark Travis , Guerrero Ricardo , Cañizales Israel , Cardenas-Callirgos Jorge Manuel , Junker Kerstin , Vallarino-Lhermitte Nathaly , Makepeace Benjamin L. , Darby Alistair C. , Foster Jeremy M. , Martin Coralie , Slatko Barton E. 
Published: June 2020

Wolbachiaare 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. DefiningWolbachia“species” is controversial and so they are commonly classified into 16 different phylogenetic lineages, termed supergroups, named A to S. However, available genomic data remains limited and not representative of the fullWolbachiadiversity; indeed, of the 24 complete genomes and 55 draft genomes ofWolbachiaavailable to date, 84% belong to supergroups A and B, exclusively composed ofWolbachiafrom arthropods.

For the current study, we took advantage of a recently developed DNA enrichment method to produce four complete genomes and two draft genomes ofWolbachiafrom filarial nematodes. Two complete genomes,wCtub andwDcau, are the smallestWolbachiagenomes sequenced to date (863,988bp and 863,427bp, 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 multi-locus system typing (MLST) approach. We also produced the first draftWolbachiagenome from a supergroup F filarial nematode representative (wMhie), two genomes from supergroup D (wLsig andwLbra) and the complete genome ofwDimm from supergroup C.

Our new data confirm the paradigm of smallerWolbachiagenomes from filarial nematodes containing low levels of transposable elements and the absence of intact bacteriophage sequences, unlike manyWolbachiafrom arthropods, where both are more abundant. However, we observe differences among theWolbachiagenomes from filarial nematodes: no global co-evolutionary pattern, strong synteny between supergroup C and supergroup JWolbachia, and more transposable elements observed in supergroup DWolbachiacompared 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 singleWolbachia-filarial nematode pattern of co-evolution or symbiotic relationship.

Graphical abstract

Repositories

Data generated are available in GenBank: BioProject PRJNA593581; BioSample SAMN13482485 forwLsig,Wolbachiaendosymbiont ofLitomosoides sigmodontis(genome: CP046577); Biosample SAMN15190311 for the nematode hostLitomosoides sigmodontis(genome: JABVXW000000000); BioSample SAMN13482488 forwDimm, Wolbachiaendosymbiont ofDirofilaria(D.)immitis(genome: CP046578); Biosample SAMN15190314 for the nematode hostDirofilaria(D.)immitis(genome: JABVXT000000000); BioSample SAMN13482046 forwCtub,Wolbachiaendosymbiont ofCruorifilaria tuberocauda(genome: CP046579); Biosample SAMN15190313 for the nematode hostCruorifilaria tuberocauda(genome: JABVXU000000000); BioSample SAMN13482057 forwDcau,Wolbachiaendosymbiont ofDipetalonema caudispina(genome: CP046580); Biosample SAMN15190312 for the nematode hostDipetalonema caudispina(genome: JABVXV000000000); BioSample SAMN13482459 forwLbra,Wolbachiaendosymbiont ofLitomosoides brasiliensis(genome: WQM000000000); Biosample SAMN15190311 for the nematode hostLitomosoides brasiliensis(genome: JABVXW000000000); BioSample SAMN13482487 forwMhie,Wolbachiaendosymbiont ofMadathamugadia hiepei(genome: WQMP00000000); Biosample SAMN15190315 for the nematode hostMadathamugadia hiepei(genome: JABVXS000000000). The raw data are available in GenBank as Sequence Read Archive (SRA): SRR10903008 to SRR10903010; SRR10902913 to SRR10902914; SRR10900508 to SRR10900511; SRR10898805 to SRR10898806.

Data summary

The authors confirm all supporting data, code and protocols have been provided within the article or through supplementary data files. Eleven Supplementary tables and two supplementary files are available with the online version of this article.

Impact Statement

Wolbachiaare endosymbiotic bacteria infecting a large range of arthropod species and two different families of nematodes, characterized by causing diverse phenotypes in their hosts, ranging from reproductive parasitism to mutualism. While availableWolbachiagenomic data are increasing, they are not representative of the fullWolbachiadiversity; indeed, 84% ofWolbachiagenomes available on the NCBI database to date belong to the two main studied clades (supergroups A and B, exclusively composed ofWolbachiafrom arthropods). The present study presents the assembly and analysis of four complete genomes and two draft genomes ofWolbachiafrom filarial nematodes. Our genomics comparisons confirm the paradigm that smallerWolbachiagenomes from filarial nematodes contain low levels of transposable elements and the absence of intact bacteriophage sequences, unlike manyWolbachiafrom arthropods. However, data show disparities among theWolbachiagenomes from filarial nematodes: no single pattern of co-evolution, stronger synteny between some clades (supergroups C and supergroup J) and more transposable elements in another clade (supergroup D). Metabolic pathway analysis indicates both highly conserved and more variable pathways, such as vitamin B biosynthesis, which might be specific to certain host-symbiont associations. Overall, there appears to be no singleWolbachia-filarial nematode pattern of symbiotic relationship.