Quek, Shannon; Cerdeira, Louise; Jeffries, Claire L; Tomlinson, Sean; Walker, Thomas; Hughes, Grant L; Heinz, Eva; (2022) Wolbachia endosymbionts in two Anopheles species indicates independent acquisitions and lack of prophage elements. Microbial genomics, 8 (4). ISSN 2057-5858 DOI: https://doi.org/10.1099/mgen.0.000805
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Abstract
<jats:p> <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> is a genus of obligate bacterial endosymbionts that infect a diverse range of arthropod species as well as filarial nematodes, with its single described species, <jats:italic> <jats:named-content content-type="species"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1006" xlink:type="simple">Wolbachia pipientis</jats:ext-link> </jats:named-content> </jats:italic>, divided into several ‘supergroups’ based on multilocus sequence typing. <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> strains in mosquitoes have been shown to inhibit the transmission of human pathogens, including <jats:italic>Plasmodium</jats:italic> malaria parasites and arboviruses. Despite their large host range, <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> strains within the major malaria vectors of the <jats:italic>Anopheles gambiae</jats:italic> and <jats:italic>Anopheles funestus</jats:italic> complexes appear at low density, established solely on PCR-based methods. Questions have been raised as to whether this represents a true endosymbiotic relationship. However, recent definitive evidence for two distinct, high-density strains of supergroup B <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> within <jats:italic>Anopheles demeilloni</jats:italic> and <jats:italic>Anopheles moucheti</jats:italic> has opened exciting possibilities to explore naturally occurring <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> endosymbionts in <jats:italic>Anopheles</jats:italic> for biocontrol strategies to block <jats:italic>Plasmodium</jats:italic> transmission. Here, we utilize genomic analyses to demonstrate that both <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> strains have retained all key metabolic and transport pathways despite their smaller genome size, with this reduction potentially attributable to degenerated prophage regions. Even with this reduction, we confirmed the presence of cytoplasmic incompatibility (CI) factor genes within both strains, with <jats:italic>w</jats:italic>AnD maintaining intact copies of these genes while the <jats:italic>cifB</jats:italic> gene was interrupted in <jats:italic>w</jats:italic>AnM, so functional analysis is required to determine whether <jats:italic>w</jats:italic>AnM can induce CI. Additionally, phylogenetic analysis indicates that these <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> strains may have been introduced into these two <jats:italic>Anopheles</jats:italic> species via horizontal transmission events, rather than by ancestral acquisition and subsequent loss events in the <jats:italic>Anopheles gambiae</jats:italic> species complex. These are the first <jats:italic> <jats:named-content content-type="genus"> <jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://doi.org/10.1601/nm.1005" xlink:type="simple">Wolbachia</jats:ext-link> </jats:named-content> </jats:italic> genomes, to our knowledge, that enable us to study the relationship between natural strain <jats:italic>Plasmodium</jats:italic> malaria parasites and their anopheline hosts.</jats:p>