<i>cifB-</i>transcript levels largely explain cytoplasmic incompatibility variation across divergent<i>Wolbachia</i>

Shropshire, J. Dylan; Hamant, Emily; Conner, William R.; Cooper, Brandon S.

doi:10.1093/pnasnexus/pgac099

Cited by 8 publications

(7 citation statements)

References 83 publications

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“…We observed CI-causing factors ( cifs ) in both the Smith+ and N101 MK assemblies [ 27 , 28 ]. cifs ( cifA/B ) are classified into 5 phylogenetic clades (Types I to V) [ 38 , 39 ]. The Smith+ genome contains 1 Type 1 and 1 Type 2 cif pair.…”

Section: Resultsmentioning

confidence: 99%

A male-killing Wolbachia endosymbiont is concealed by another endosymbiont and a nuclear suppressor

et al. 2023

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Bacteria that live inside the cells of insect hosts (endosymbionts) can alter the reproduction of their hosts, including the killing of male offspring (male killing, MK). MK has only been described in a few insects, but this may reflect challenges in detecting MK rather than its rarity. Here, we identify MK Wolbachia at a low frequency (around 4%) in natural populations of Drosophila pseudotakahashii. MK Wolbachia had a stable density and maternal transmission during laboratory culture, but the MK phenotype which manifested mainly at the larval stage was lost rapidly. MK Wolbachia occurred alongside a second Wolbachia strain expressing a different reproductive manipulation, cytoplasmic incompatibility (CI). A genomic analysis highlighted Wolbachia regions diverged between the 2 strains involving 17 genes, and homologs of the wmk and cif genes implicated in MK and CI were identified in the Wolbachia assembly. Doubly infected males induced CI with uninfected females but not females singly infected with CI-causing Wolbachia. A rapidly spreading dominant nuclear suppressor genetic element affecting MK was identified through backcrossing and subsequent analysis with ddRAD SNPs of the D. pseudotakahashii genome. These findings highlight the complexity of nuclear and microbial components affecting MK endosymbiont detection and dynamics in populations and the challenges of making connections between endosymbionts and the host phenotypes affected by them.

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Section: Resultsmentioning

confidence: 99%

A male-killing Wolbachia endosymbiont is concealed by another endosymbiont and a nuclear suppressor

et al. 2023

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“…The results showed that the lDDT scores of all of the six Cif proteins of w Ccep and w Mel ranged between 68.4 and 84.0, suggesting a confident structural prediction based on the full‐length sequences using the AlphaFold programme, except for CifB I w Mel containing a DUB domain with a low predicted mass (Table 3; Figure S4). Only two PD‐(D/E)XK‐nuclease domains of CifB were analysed because they were shared across all types of Cif proteins (Shropshire et al, 2022), and it was difficult to make a direct determination of the structure of CifB w Mel because its expression in Escherichia coli was poor (Wang et al, 2022). To evaluate the similarity between the tertiary structures of CIF proteins, the template modelling (TM) scores were calculated (Xu & Zhang, 2010).…”

Section: Resultsmentioning

confidence: 99%

“…CIF proteins were preliminarily analysed using the SMART programme (http://smart.embl-heidelberg.de/; Schultz et al, 1998). The proteins were further analysed for the presence of putative domains using the HHpred protein domain prediction tool (https://toolkit.tuebingen.mpg.de/#/tools/hhpred) (Söding et al, 2005; Zimmermann et al, 2018) with default parameters, and annotations with p > 80% were recorded (Shropshire et al, 2022). The databases SCOPe70 (v.2.07), Pfam (v.33.1), SMART (v6.0) and COG/KOG (v1.0) (Lindsey et al, 2018; Martinez et al, 2022) were used to confirm SMART‐identified domains and identify additional domain structures.…”

Section: Methodsmentioning

confidence: 99%

Transinfected Wolbachia strains induce a complex of cytoplasmic incompatibility phenotypes: Roles of CI factor genes

Dong

Zhong³

et al. 2023

Environ Microbiol Rep

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Wolbachia can modulate the reproductive development of their hosts in multiple modes, and cytoplasmic incompatibility (CI) is the most well‐studied phenotype. The whitefly Bemisia tabaci is highly receptive to different Wolbachia strains: wCcep strain from the rice moth Corcyra cephalonica and wMel strain from the fruit fly Drosophila melanogaster could successfully establish and induce CI in transinfected whiteflies. Nevertheless, it is unknown what will happen when these two exogenous Wolbachia strains are co‐transinfected into a new host. Here, we artificially transinferred wCcep and wMel into the whitefly and established double‐ and singly‐transinfected B. tabaci isofemale lines. Reciprocal crossing experiments showed that wCcep and wMel induced a complex of CI phenotypes in the recipient host, including unidirectional and bidirectional CI. We next sequenced the whole genome of wCcep and performed a comparative analysis of the CI factor genes between wCcep and wMel, indicating that their cif genes were phylogenetically and structurally divergent, which can explain the crossing results. The amino acid sequence identity and structural features of Cif proteins may be useful parameters for predicting their function. Structural comparisons between CifA and CifB provide valuable clues for explaining the induction or rescue of CI observed in crossing experiments between transinfected hosts.

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“…Our analyses discovered CI-causing factors ( cifs ) in both the Smith+ and N101 MK draft assemblies [26, 27]. cifs ( cifA/B ) are classified into five phylogenetic clades (Types I–V) [28, 29]. The Smith+ genome contains one set of Type 1 cif loci and one set of the Type 2 loci.…”

Section: Resultsmentioning

confidence: 99%

Hidden endosymbionts: A male-killer concealed by another endosymbiont and a nuclear suppressor

Richardson

Ross

Cooper

et al. 2022

Preprint

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Maternally transmitted endosymbiotic bacteria that cause male killing (MK) have only been described from a few insects, but this may reflect challenges in their detection rather than a rarity of MK. Here we identify MKWolbachiain populations ofDrosophila pseudotakahashii, present at a low frequency (around 4%) in natural populations and previously undetected due to a different fixedWolbachiastrain in this species expressing a different reproductive manipulation, cytoplasmic incompatibility (CI). The MK phenotype was eliminated after tetracycline treatment that removedWolbachia. Molecular analyses indicated the MK phenotype to be expressed when a secondWolbachiastrain was present alongside the CIWolbachia. A genomic analysis highlightedWolbachiaregions diverged between the strains involving 17 genes and also identified theWolbachiaas representing an outgroup to a clade ofWolbachiainfectingmelanogaster-group species, includingwRi-like andwMel-like strains. Doubly infected males induced CI with uninfected females but not females singly infected with CI-causingWolbachia. The MK phenotype manifested at the larval stage and was transmitted maternally at a high fidelity but with occasional loss of the MKWolbachiastrain. A rapidly spreading dominant nuclear suppressor genetic element affecting MK was identified through backcrossing and subsequent analysis with ddRAD SNPs of theD. pseudotakahashiigenome. These findings highlight the complexity of nuclear and microbial components affecting MK endosymbiont detection and dynamics in populations, and the challenges of making connections between endosymbionts and the host phenotypes affected by them.

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cifB-transcript levels largely explain cytoplasmic incompatibility variation across divergentWolbachia

Cited by 8 publications

References 83 publications

A male-killing Wolbachia endosymbiont is concealed by another endosymbiont and a nuclear suppressor

A male-killing Wolbachia endosymbiont is concealed by another endosymbiont and a nuclear suppressor

Transinfected Wolbachia strains induce a complex of cytoplasmic incompatibility phenotypes: Roles of CI factor genes

Hidden endosymbionts: A male-killer concealed by another endosymbiont and a nuclear suppressor

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