Multiple long-range host shifts of major Wolbachia supergroups infecting arthropods

Gomes, Tiago M. F. F.; Wallau, Gabriel Luz; Loreto, Élgion Lúcio Silva

doi:10.1038/s41598-022-12299-x

Cited by 12 publications

(6 citation statements)

References 42 publications

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“…Also, we used an uncalibrated host phylogeny, as it is commonly done, but it would be interesting for future studies to explore the effect of host phylogeny calibration on the detection of phylosymbiosis. This result is in broad agreement with phylogenomic analysis documenting a lack of congruency between host and Wolbachia phylogenies or genetic divergences [ 69 , 70 ] but also with observations that Spiroplasma can switch between hosts in the laboratory [ 71 ]. Altogether, this suggests that endosymbionts can be easily swapped between host species across evolutionary time (a pattern sometimes referred to as « horizontal transfer »).…”

Section: Discussionsupporting

confidence: 90%

Contrasted host specificity of gut and endosymbiont bacterial communities in alpine grasshoppers and crickets

Mazel,

Pitteloud,

Guisan

et al. 2024

ISME Communications

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Bacteria colonize the body of macroorganisms to form associations ranging from parasitic to mutualistic. Endosymbiont and gut symbiont community are distinct microbiomes whose compositions are influenced by host ecology and evolution. Although the composition of horizontally acquired symbiont communities can correlate to host species identity (i.e., harbor host specificity) and host phylogeny (i.e., harbor phylosymbiosis), we hypothesize that the microbiota structure of vertically inherited symbionts (e.g., endosymbionts like Wolbachia) is more strongly associated with the host species identity and phylogeny than horizontally acquired symbionts (e.g., most gut symbionts). Here, using 16S metabarcoding on 336 guts from 24 orthopteran species (grasshoppers and crickets) in the Alps, we observed that microbiota correlated to host species identity, i.e., hosts from the same species had more similar microbiota than hosts from different species. This effect was ~5 times stronger for endosymbionts than for putative gut symbionts. While elevation correlated with microbiome composition, we did not detect phylosymbiosis for endosymbionts and putative gut symbionts: closely related host species did not harbor more similar microbiota than distantly related species. Our findings indicate that gut microbiota of studied orthopteran species is more correlated to host identity and habitat than to the host phylogeny. The higher specificity in endosymbionts corroborates the idea that -everything else being equal- vertically transmitted microbes harbor stronger specificity signal, but the absence of phylosymbiosis suggests that specificity changes quickly on evolutionary time scales.

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Section: Discussionsupporting

confidence: 90%

Contrasted host specificity of gut and endosymbiont bacterial communities in alpine grasshoppers and crickets

Mazel,

Pitteloud,

Guisan

et al. 2024

ISME Communications

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“…Wolbachia strains are divided into 20 supergroups, ranging from A to U (G was not considered anymore) which diverged around 100 million years ago, first in filarial nematodes and then infecting arthropods [ 63 ]. In this study we found F supergroup in the cockroaches which is also found in distantly related host species including nematodes and domestic indoor pests ( Cimex , Supella and Blattella ).…”

Section: Discussionmentioning

confidence: 99%

“…In this study we found F supergroup in the cockroaches which is also found in distantly related host species including nematodes and domestic indoor pests ( Cimex , Supella and Blattella ). Wolbachia is transmitted either vertically between host generations or horizontally to other individuals and species through a mechanism called host shift (HS) [ 63 – 65 ].…”

Section: Discussionmentioning

confidence: 99%

Wolbachia infection in native populations of Blattella germanica and Periplaneta americana

et al. 2023

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Cockroaches are significant pests worldwide, being important in medical, veterinary, and public health fields. Control of cockroaches is difficult because they have robust reproductive ability and high adaptability and are resistant to many insecticides. Wolbachia is an endosymbiont bacterium that infects the reproductive organs of approximately 70% of insect species and has become a promising biological agent for controlling insect pests. However, limited data on the presence or strain typing of Wolbachia in cockroaches are available. PCR amplification and sequencing of the wsp and gltA genes were used to study the presence, prevalence and molecular typing of Wolbachia in two main cockroach species, Blattella germanica (German cockroach) and Periplaneta americana (American cockroach), from different geographical locations of Iran. The Wolbachia endosymbiont was found only in 20.6% of German cockroaches while it was absent in American cockroach samples. Blast search and phylogenetic analysis revealed that the Wolbachia strain found in the German cockroach belongs to Wolbachia supergroup F. Further studies should investigate the symbiotic role of Wolbachia in cockroaches and determine whether lack of Wolbachia infection may increase this insect’s ability to tolerate or acquire various pathogens. Results of our study provide a foundation for continued work on interactions between cockroaches, bacterial endosymbionts, and pathogens.

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“…500 mya [1,2] , Wolbachia endosymbionts evolved (ca. 100-200 mya [3] ) and spread to infect a high proportion of these hosts [4][5][6] . Following horizontal transmission to a new host and establishment of a stable infection, Wolbachia targets the host germline to achieve vertical transmission from one host generation to the next [4,7,8] .…”

Section: Introductionmentioning

confidence: 99%

MixedWolbachiainfections resolve rapidly duringin vitroevolution

Mirchandani,

Wang,

Jacobs

et al. 2024

Preprint

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The intracellular symbiontWolbachia pipientisevolved after the divergence of arthropods and nematodes, but it reached high prevalence in many of these taxa through its abilities to infect new hosts and their germlines. Some strains exhibit long-term patterns of co-evolution with their hosts, while other strains are capable of switching hosts. This makes strain selection an important factor in symbiont-based biological control. However, little is known about the ecological and evolutionary interactions that occur when a promiscuous strain colonizes an infected host. Here, we study what occurs when two strains come into contact in host cells following horizontal transmission and infection. We focus on the faithful wMel strain fromDrosophila melanogasterand the promiscuous wRi strain fromDrosophila simulansusing anin vitrocell culture system with multiple host cell types and combinatorial infection states. MixingD. melanogastercell lines stably infected with wMel and wRi revealed that wMel outcompetes wRi quickly and reproducibly. Furthermore, wMel was able to competitively exclude wRi even from minuscule starting quantities, indicating that this is a nearly deterministic outcome, independent of the starting infection frequency. This competitive advantage was not exclusive to wMel’s nativeD. melanogastercell background, as wMel also outgrew wRi inD. simulanscells. Overall, wRi is less adept at in vitro growth and survival than wMel and its in vivo state, revealing differences between cellular and humoral regulation. These attributes may underlie the observed low rate of mixed infections in nature and the relatively rare rate of host-switching in most strains. Our in vitro experimental framework for estimating cellular growth dynamics ofWolbachiastrains in different host species, tissues, and cell types provides the first strategy for parameterizing endosymbiont and host cell biology at high resolution. This toolset will be crucial to our application of these bacteria as biological control agents in novel hosts and ecosystems.

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Multiple long-range host shifts of major Wolbachia supergroups infecting arthropods

Cited by 12 publications

References 42 publications

Contrasted host specificity of gut and endosymbiont bacterial communities in alpine grasshoppers and crickets

Contrasted host specificity of gut and endosymbiont bacterial communities in alpine grasshoppers and crickets

Wolbachia infection in native populations of Blattella germanica and Periplaneta americana

MixedWolbachiainfections resolve rapidly duringin vitroevolution

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