Detection and Characterization of Wolbachia Infections in Natural Populations of Aphids: Is the Hidden Diversity Fully Unraveled?

Augustinos, Antonios A.; Santos-García, Diego; Dionyssopoulou, Eva; Moreira, Marta; Papapanagiotou, Aristeidis P.; Scarvelakis, Marios; Doudoumis, Vangelis; Ramos, Silvia; Aguiar, A. M. Franquinho; Borges, Paulo A. V.; Khadem, Mahnaz; Latorre, Amparo; Tsiamis, George; Bourtzis, Kostas

doi:10.1371/journal.pone.0028695

Cited by 168 publications

(200 citation statements)

References 99 publications

(111 reference statements)

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“…Wolbachia strains are represented with the name of their host species. The scale value of 0.02 is marked with a red line, because the value was considered a threshold to establish new supergroups for Wolbachia (Augustinos et al., 2011). Sequence pairs concerning about w M yos infecting Mes.…”

Section: Resultsmentioning

confidence: 99%

Revisiting the phylogeny ofWolbachiain Collembola

Chen

et al. 2017

Ecology and Evolution

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The endosymbiont Wolbachia has been detected in a few parthenogenetic collembolans sampled in Europe and America, including three species of Poduromorpha, two species of Entomobryomorpha, and two species of Neelipleona. Based on 16S rRNA and ftsZ gene sequences, most of the Wolbachia infecting parthenogenetic collembolans were characterized as members of supergroup E and showed concordant phylogeny with their hosts. However, the two neelipleonan symbionts form another unique group, indicating that Wolbachia has infected parthenogenetic collembolans multiple times. In this study, five parthenogenetic collembolan species were identified as hosts of Wolbachia, and four new Wolbachia strains were reported for four collembolan species sampled in China, respectively, including a neelipleonan strain from Megalothorax incertus (wMinc). Our results demonstrated that the Wolbachia multilocus sequence typing (MLST) system is superior to the 16S rRNA + ftsZ approach for phylogenetic analyses of collembolan Wolbachia. The MLST system assigned these Wolbachia of parthenogenetic collembolans to supergroup E as a unique clade, which included wMinc, supporting the monophyletic origin of Wolbachia in parthenogenetic collembolan species. Moreover, our data suggested supergroup E as one of the most divergent lineages in Wolbachia and revealed the discrepancy between the phylogenies of Wolbachia from parthenogenetic collembolans and their hosts, which may result from the high level of genetic divergence between collembolan Wolbachia, in association with the geographic differentiation of their hosts, or the possible horizontal transmission of Wolbachia between different collembolan species.

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Section: Resultsmentioning

confidence: 99%

Revisiting the phylogeny ofWolbachiain Collembola

Chen

et al. 2017

Ecology and Evolution

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“…It should be stressed that an earlier molecular analyses did not detect Wolbachia in aphids (Tsuchida et al, 2002). However, recent extensive studies have indicated that this bacterium occurs sporadically in some populations of representatives of several aphid families (Wang et al, 2009;Augustinos et al, 2011).…”

Section: Discussionmentioning

confidence: 96%

Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission

Michalik¹,

Szklarzewicz²,

Jankowska³

et al. 2014

Eur. J. Entomol.

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Abstract. The ultrastructure, distribution and transovarial transmission of endosymbiotic bacteria in representatives of six aphid families: Eriosomatidae (Pemphigus spyrothecae, Prociphilus fraxini), Anoeciidae [Anoecia (Anoecia) corni], Drepanosiphidae [Mindarus abietinus, Sipha (Rungsia) maydis, Clethrobius comes, Myzocallis (Lineomyzocallis) walshii], Thelaxidae (Thelaxes dryophila), Aphididae (Delphiniobium junackianum, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria) and Lachnidae (Schizolachnus pineti, Eulachnus rileyi) were studied at the ultrastructural level. The ovaries of aphids are accompanied by large organs termed bacteriomes that consist of giant cells termed bacteriocytes. The bacteriocyte cytoplasm is tightly packed with endosymbiotic bacteria. Ultrastructural observations have shown that the bacteria Buchnera aphidicola (primary symbiont of aphids) present in various species are characterized by significant differences in both size and organization of their cytoplasm. In the aphids, Prociphilus fraxini, Sipha (Rungsia) maydis, Thelaxes dryophila, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria, Eulachnus rileyi and Schizolachnus pineti, in addition to Buchnera aphidicola, secondary endosymbionts are also present. The bacteriocytes containing secondary endosymbionts are less numerous than those with Buchnera. In Eulachnus rileyi (Lachnidae), in addition to primary and secondary endosymbionts, there is a third type of microorganism. In all species examined both the primary and secondary endosymbionts are transovarially transmitted from mother to offspring.

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“…The clade containing Wolbachia pipientis is divided into 11 to 13 supergroups, depending on the study (1,3,18). Wolbachia bacteria are maternally transmitted reproductive parasites (19,27).…”

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confidence: 99%

Association of a New Wolbachia Strain with, and Its Effects on, Leptopilina victoriae, a Virulent Wasp Parasitic to Drosophila spp

Gueguen

Onemola

Govind

2012

Appl Environ Microbiol

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bWolbachia bacteria are ubiquitous intracellular bacteria of arthropods. Often considered reproductive parasites, they can benefit certain host species. We describe a new Wolbachia strain from Leptopilina victoriae, a Drosophila wasp. The strain is closely related to Wolbachia from Culex sp. Located to the posterior poles of oocytes, it manipulates its host's reproduction by inducing a male development type of cytoplasmic incompatibility. We also report its diverse effects on the wasp's life history traits.T he alphaproteobacterium Wolbachia pipientis is an intracellular symbiont found in many arthropod species (12). The clade containing Wolbachia pipientis is divided into 11 to 13 supergroups, depending on the study (1,3,18). Wolbachia bacteria are maternally transmitted reproductive parasites (19,27). A common effect of Wolbachia is the induction of cytoplasmic incompatibility (CI). CI is observed when Wolbachia-infected males mate with either females without Wolbachia or females carrying a different Wolbachia strain. Such reproductive incompatibility gives a fitness advantage to infected females and results in an increase in Wolbachia-infected individuals in the population (27). Wolbachia can also induce male killing, thelytokous parthenogenesis, and feminization of genetic males (21,27). In some cases, Wolbachia bacteria impose a cost on the fitness of their hosts (5, 6, 17). Conversely, Wolbachia bacteria can protect their hosts against pathogens or improve their fecundity (9,11,22,24). Overall, the biological effects of Wolbachia are strain and host specific.A Wolbachia strain, belonging to the B supergroup, has been identified in the parasitoid wasp Leptopilina victoriae (7), but little is known about its exact phylogenetic position and effects on L. victoriae. In contrast, the identity and the effects of Wolbachia in its sister species Leptopilina heterotoma have been well characterized (6,23,25).In this study, we show that Wolbachia from L. victoriae constitutes a novel strain type which is related to a strain of Wolbachia from Culex sp. It induces a male development type of CI and also affects size, developmental time, and fecundity of L. victoriae. The range of Drosophila species that L. victoriae attacks is limited, and this host range appears not to be affected by Wolbachia. These results advance our understanding of the biology of L. victoriae in relation to its exceptionally well-studied Drosophila host.Endosymbiotic bacteria of L. victoriae. Our laboratory culture of L. victoriae (16,20) was screened for the presence of five endosymbiotic bacteria known to influence host biology and reproduction, Wolbachia, Cardinium, Arsenophonus, Rickettsia, and Spiroplasma, as described previously (10, 15). Only one strain of Wolbachia was found to infect L. victoriae.A new Wolbachia strain type in L. victoriae. The five genes for multilocus sequence typing (MLST) of L. victoriae Wolbachia (gatB, coxA, hcpA, ftsZ, and fbpA) were sequenced. On the basis of a comparison to the Wolbachia MLST database (13; http: ...

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Detection and Characterization of Wolbachia Infections in Natural Populations of Aphids: Is the Hidden Diversity Fully Unraveled?

Cited by 168 publications

References 99 publications

Revisiting the phylogeny ofWolbachiain Collembola

Revisiting the phylogeny ofWolbachiain Collembola

Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission

Association of a New Wolbachia Strain with, and Its Effects on, Leptopilina victoriae, a Virulent Wasp Parasitic to Drosophila spp

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