scholarly journals Wolbachia Transfer from Drosophila melanogaster into D. simulans: Host Effect and Cytoplasmic Incompatibility Relationships

Genetics ◽  
1998 ◽  
Vol 150 (1) ◽  
pp. 227-237 ◽  
Author(s):  
Denis Poinsot ◽  
Kostas Bourtzis ◽  
George Markakis ◽  
Charalambos Savakis ◽  
Hervé Merçot
Keyword(s):  
Drosophila Melanogaster ◽  
Cytoplasmic Incompatibility ◽  
Bacterial Load ◽  
Embryonic Mortality ◽  
Isofemale Line ◽  
Young Males ◽  
Arthropod Species ◽  
Asymmetrical Pattern ◽  
Reproductive Incompatibility ◽  
Host Effect

Abstract Wolbachia are maternally transmitted endocellular bacteria causing a reproductive incompatibility called cytoplasmic incompatibility (CI) in several arthropod species, including Drosophila. CI results in embryonic mortality in incompatible crosses. The only bacterial strain known to infect Drosophila melanogaster (wDm) was transferred from a D. melanogaster isofemale line into uninfected D. simulans isofemale lines by embryo microinjections. Males from the resulting transinfected lines induce >98% embryonic mortality when crossed with uninfected D. simulans females. In contrast, males from the donor D. melanogaster line induce only 18–32% CI on average when crossed with uninfected D. melanogaster females. Transinfected D. simulans lines do not differ from the D. melanogaster donor line in the Wolbachia load found in the embryo or in the total bacterial load of young males. However, >80% of cysts are infected by Wolbachia in the testes of young transinfected males, whereas only 8% of cysts are infected in young males from the D. melanogaster donor isofemale line. This difference might be caused by physiological differences between hosts, but it might also involve tissue-specific control of Wolbachia density by D. melanogaster. The wDm-transinfected D. simulans lines are unidirectionally incompatible with strains infected by the non-CI expressor Wolbachia strains wKi, wMau, or wAu, and they are bidirectionally incompatible with strains infected by the CI-expressor Wolbachia strains wHa or wNo. However, wDm-infected males do not induce CI toward females infected by the CI-expressor strain wRi, which is found in D. simulans continental populations, while wRi-infected males induce partial CI toward wDm-infected females. This peculiar asymmetrical pattern could reflect an ongoing divergence between the CI mechanisms of wRi and wDm. It would also confirm other results indicating that the factor responsible for CI induction in males is distinct from the factor responsible for CI rescue in females.

scholarly journals Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia

2002 ◽  
Vol 80 (2) ◽  
pp. 79-87 ◽  
Author(s):  
K. TRACY REYNOLDS ◽  
ARY A. HOFFMANN
Keyword(s):  
Drosophila Melanogaster ◽  
Host Species ◽  
Cytoplasmic Incompatibility ◽  
Strain Differences ◽  
Large Impact ◽  
Young Males ◽  
Male Age ◽  
Weak Expression ◽  
Host Effects

In Drosophila melanogaster, the maternally inherited endocellular microbe Wolbachia causes cytoplasmic incompatibility (CI) in crosses between infected males and uninfected females. CI results in a reduction in the number of eggs that hatch. The level of CI expression in this species has been reported as varying from partial (a few eggs fail to hatch) to nonexistent (all eggs hatch). We show that male age in this host species has a large impact on the level of CI exhibited and explains much of this variability. Strong CI is apparent when young males are used in crosses. CI declines rapidly with male age, particularly when males are repeatedly mated. Wolbachia from a Canton S line that was previously reported as not causing CI does in fact induce CI when young males are used in crosses, albeit at a weaker level than in other D. melanogaster strains. The strain differences in CI expression are due to host background effects rather than differences in Wolbachia strains. These results highlight the importance of undertaking crosses with a range of male ages and nuclear backgrounds before ascribing particular host phenotypes to Wolbachia strains.

scholarly journals Pathogenicity of Life-Shortening Wolbachia in Aedes albopictus after Transfer from Drosophila melanogaster

2009 ◽  
Vol 75 (24) ◽  
pp. 7783-7788 ◽  
Author(s):  
Eunho Suh ◽  
David R. Mercer ◽  
Yuqing Fu ◽  
Stephen L. Dobson
Keyword(s):  
Drosophila Melanogaster ◽  
Aedes Albopictus ◽  
Age Structure ◽  
Cytoplasmic Incompatibility ◽  
Fitness Cost ◽  
Embryonic Mortality ◽  
Typical Pattern ◽  
Interspecific Transfer ◽  
Selection Of

ABSTRACT Maternally inherited Wolbachia bacteria have evolved mechanisms to manipulate the reproduction of their invertebrate hosts, promoting infection spread. A high fitness cost to the host is maladaptive for obligate endosymbionts, and prior studies show rapid selection of new Wolbachia associations toward commensal or mutualistic symbioses. Here, wMelPop Wolbachia is transferred from Drosophila melanogaster into the mosquito Aedes albopictus. Characterization of the resulting strain provides an extreme example of Wolbachia as a pathogen. In addition to reduced longevity and fecundity, abnormally high Wolbachia density is associated with embryonic mortality that masks the typical pattern of cytoplasmic incompatibility. The results are consistent with earlier reports that show unpredictable shifts in the Wolbachia phenotype after interspecific transfer, which can complicate proposed strategies to modify the age structure of medically important vector populations.

scholarly journals Paternal Grandmother Age Affects the Strength of Wolbachia-Induced Cytoplasmic Incompatibility in Drosophila melanogaster

mBio ◽  
2019 ◽  
Vol 10 (6) ◽  
Author(s):  
Emily M. Layton ◽  
Jungmin On ◽  
Jessamyn I. Perlmutter ◽  
Seth R. Bordenstein ◽  
J. Dylan Shropshire
Keyword(s):  
Drosophila Melanogaster ◽  
Cytoplasmic Incompatibility ◽  
Genetic Model ◽  
Relative Fitness ◽  
Content Type ◽  
Adult Sons ◽  
Fitness Advantage ◽  
Arthropod Species ◽  
Obligate Intracellular Bacteria ◽  
Methodological Advance

ABSTRACT Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. As the most abundant maternally inherited microbe in animals, Wolbachia manipulate host reproduction via reproductive parasitism strategies, including cytoplasmic incompatibility (CI). CI manifests as embryonic death when Wolbachia-modified sperm fertilize uninfected eggs but not maternally infected eggs. Thus, CI can provide a relative fitness advantage to Wolbachia-infected females and drive the infection through a population. In the genetic model Drosophila melanogaster, the Wolbachia strain wMel induces variable CI, making mechanistic studies in D. melanogaster cumbersome. Here, we demonstrate that sons of older paternal D. melanogaster grandmothers induce stronger CI than sons of younger paternal grandmothers, and we term this relationship the “paternal grandmother age effect” (PGAE). Moreover, the embryos and adult sons of older D. melanogaster grandmothers have higher Wolbachia densities, correlating with their ability to induce stronger CI. In addition, we report that Wolbachia density positively correlates with female age and decreases after mating, suggesting that females transmit Wolbachia loads that are proportional to their own titers. These findings reveal a transgenerational impact of age on wMel-induced CI, elucidate Wolbachia density dynamics in D. melanogaster, and provide a methodological advance to studies aimed at understanding wMel-induced CI in the D. melanogaster model. IMPORTANCE Unidirectional cytoplasmic incompatibility (CI) results in a postfertilization incompatibility between Wolbachia-infected males and uninfected females. CI contributes to reproductive isolation between closely related species and is used in worldwide vector control programs to drastically lower arboviral vector population sizes or to replace populations that transmit arboviruses with those resistant to transmission. Despite decades of research on the factors that influence CI, penetrance is often variable under controlled laboratory conditions in various arthropods, suggesting that additional variables influence CI strength. Here, we demonstrate that paternal D. melanogaster grandmother age influences the strength of CI induced by their sons. Older D. melanogaster females have higher Wolbachia densities and produce offspring with higher Wolbachia densities that associate with stronger CI. This work reveals a multigenerational impact of age on CI and expands our understanding of host-Wolbachia interactions and the biology of CI induced by the Wolbachia strain infecting the most widely used arthropod model, D. melanogaster.

scholarly journals Wolbachia affect behavior and possibly reproductive compatibility but not thermoresistance, fecundity, and morphology in a novel transinfected host, Drosophila nigrosparsa

2020 ◽  
Author(s):  
Matsapume Detcharoen ◽  
Wolfgang Arthofer ◽  
Francis M. Jiggins ◽  
Florian M. Steiner ◽  
Birgit C. Schlick-Steiner
Keyword(s):  
Drosophila Melanogaster ◽  
Cold Tolerance ◽  
Horizontal Transfer ◽  
Cytoplasmic Incompatibility ◽  
Wing Morphology ◽  
Species Migration ◽  
Arthropod Species ◽  
Reproductive Compatibility ◽  
Locomotor Activities ◽  
Native Host

AbstractWolbachia, intracellular endosymbionts, are estimated to infect about half of all arthropod species. These bacteria manipulate their hosts in various ways for their maximum benefits. The rising global temperature may accelerate species migration and, thus, horizontal transfer of Wolbachia may occur across species previously not in contact. We transinfected and then cured the alpine fly Drosophila nigrosparsa with Wolbachia strain wMel to study its effects on this species. We found low Wolbachia titer, possibly cytoplasmic incompatibility, and an increase in locomotion of both infected larvae and adults compared with cured ones. However, no change in fecundity, no impact on heat and cold tolerance, and no change in wing morphology were observed. Although Wolbachia increased locomotor activities in this species, we conclude that D. nigrosparsa may not benefit from the infection. Still, D. nigrosparsa can serve as a host for Wolbachia because vertical transmission is possible but may not be as high as in the native host of wMel, Drosophila melanogaster.

scholarly journals On the mod resc Model and the Evolution of Wolbachia Compatibility Types

Genetics ◽  
2001 ◽  
Vol 159 (4) ◽  
pp. 1415-1422 ◽  
Author(s):  
Sylvain Charlat ◽  
Claire Calmet ◽  
Hervé Merçot
Keyword(s):  
Cytoplasmic Incompatibility ◽  
Natural Populations ◽  
Evolutionary Process ◽  
Embryonic Mortality ◽  
Step Process ◽  
Zygote Development ◽  
Specific Manner

Abstract Cytoplasmic incompatibility (CI) is induced by the endocellular bacterium Wolbachia. It results in an embryonic mortality occurring when infected males mate with uninfected females. The mechanism involved is currently unknown, but the mod resc model allows interpretation of all observations made so far. It postulates the existence of two bacterial functions: modification (mod) and rescue (resc). The mod function acts in the males' germline, before Wolbachia are shed from maturing sperm. If sperm is affected by mod, zygote development will fail unless resc is expressed in the egg. Interestingly, CI is also observed in crosses between infected males and infected females when the two partners bear different Wolbachia strains, demonstrating that mod and resc interact in a specific manner: Two Wolbachia strains are compatible with each other only if they harbor the same compatibility type. Here we focus on the evolutionary process involved in the emergence of new compatibility types from ancestral ones. We argue that new compatibility types are likely to evolve under a wider range of conditions than previously thought, through a two-step process. First, new mod variants can arise by mutation and spread by drift. This is possible because mod is expressed in males and Wolbachia is transmitted by females. Second, once such a mod variant achieves a certain frequency, it can create the conditions for the deterministic invasion of a new resc variant, allowing the invasion of a new mod resc pair. Furthermore, we show that a stable polymorphism might be maintained in natural populations, allowing the long-term existence of “suicidal” Wolbachia strains.

scholarly journals One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster

2018 ◽  
Author(s):  
J. Dylan Shropshire ◽  
Jungmin On ◽  
Emily M. Layton ◽  
Helen Zhou ◽  
Seth R. Bordenstein
Keyword(s):  
Drosophila Melanogaster ◽  
Vector Control ◽  
Genetic Basis ◽  
Cytoplasmic Incompatibility ◽  
Embryo Rescue ◽  
Field Trials ◽  
Current Control ◽  
Drive System ◽  
World Health ◽  
Fitness Advantage

AbstractWolbachia are maternally-inherited, intracellular bacteria at the forefront of vector control efforts to curb arbovirus transmission. In international field trials, the cytoplasmic incompatibility (CI) drive system of wMel Wolbachia is deployed to replace target vector populations, whereby a Wolbachia– induced modification of the sperm genome kills embryos. However, Wolbachia in the embryo rescue the sperm genome impairment, and therefore CI results in a strong fitness advantage for infected females that transmit the bacteria to offspring. The two genes responsible for the wMel-induced sperm modification of CI, cifA and cifB, were recently identified in the eukaryotic association module of prophage WO, but the genetic basis of rescue is unresolved. Here we use transgenic and cytological approaches to demonstrate that cifA independently rescues CI and nullifies embryonic death caused by wMel Wolbachia in Drosophila melanogaster. Discovery of cifA as the rescue gene and previously one of two CI induction genes establishes a new ‘Two-by-One’ model that underpins the genetic basis of CI. Results highlight the central role of prophage WO in shaping Wolbachia phenotypes that are significant to arthropod evolution and vector control.Significance StatementThe World Health Organization recommended pilot deployment of Wolbachia-infected mosquitoes to curb viral transmission to humans. Releases of mosquitoes are underway worldwide because Wolbachia can block replication of these pathogenic viruses and deterministically spread by a drive system termed cytoplasmic incompatibility (CI). Despite extensive research, the underlying genetic basis of CI remains only half-solved. We recently reported that two prophage WO genes recapitulate the modification component of CI in a released strain for vector control. Here we show that one of these genes underpins rescue of CI. Together, our results reveal the complete genetic basis of this selfish trait and pave the way for future studies exploring WO prophage genes as adjuncts or alternatives to current control efforts.

scholarly journals The Biochemistry of Cytoplasmic Incompatibility Caused by Endosymbiotic Bacteria

Genes ◽  
2020 ◽  
Vol 11 (8) ◽  
pp. 852
Author(s):  
Hongli Chen ◽  
Mengwen Zhang ◽  
Mark Hochstrasser
Keyword(s):  
Molecular Mechanisms ◽  
Protein Pair ◽  
Cytoplasmic Incompatibility ◽  
Wolbachia Infection ◽  
Threshold Level ◽  
Upstream Gene ◽  
Arthropod Species ◽  
Bacterial Endosymbionts ◽  
Inducing Factors ◽  
New Research

Many species of arthropods carry maternally inherited bacterial endosymbionts that can influence host sexual reproduction to benefit the bacterium. The most well-known of such reproductive parasites is Wolbachia pipientis. Wolbachia are obligate intracellular α-proteobacteria found in nearly half of all arthropod species. This success has been attributed in part to their ability to manipulate host reproduction to favor infected females. Cytoplasmic incompatibility (CI), a phenomenon wherein Wolbachia infection renders males sterile when they mate with uninfected females, but not infected females (the rescue mating), appears to be the most common. CI provides a reproductive advantage to infected females in the presence of a threshold level of infected males. The molecular mechanisms of CI and other reproductive manipulations, such as male killing, parthenogenesis, and feminization, have remained mysterious for many decades. It had been proposed by Werren more than two decades ago that CI is caused by a Wolbachia-mediated sperm modification and that rescue is achieved by a Wolbachia-encoded rescue factor in the infected egg. In the past few years, new research has highlighted a set of syntenic Wolbachia gene pairs encoding CI-inducing factors (Cifs) as the key players for the induction of CI and its rescue. Within each Cif pair, the protein encoded by the upstream gene is denoted A and the downstream gene B. To date, two types of Cifs have been characterized based on the enzymatic activity identified in the B protein of each protein pair; one type encodes a deubiquitylase (thus named CI-inducing deubiquitylase or cid), and a second type encodes a nuclease (named CI-inducing nuclease or cin). The CidA and CinA proteins bind tightly and specifically to their respective CidB and CinB partners. In transgenic Drosophila melanogaster, the expression of either the Cid or Cin protein pair in the male germline induces CI and the expression of the cognate A protein in females is sufficient for rescue. With the identity of the Wolbachia CI induction and rescue factors now known, research in the field has turned to directed studies on the molecular mechanisms of CI, which we review here.

Small RNA analysis provides new insights into cytoplasmic incompatibility in Drosophila melanogaster induced by Wolbachia

2019 ◽  
Vol 118 ◽  
pp. 103938 ◽  
Author(s):  
Ya Zheng ◽  
Wei Shen ◽  
Jie Bi ◽  
Meng-Yan Chen ◽  
Rui-Fang Wang ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Small Rna ◽  
Cytoplasmic Incompatibility ◽  
Rna Analysis

scholarly journals Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

mSystems ◽  
2020 ◽  
Vol 5 (1) ◽  
Author(s):  
Jessamyn I. Perlmutter ◽  
Jane E. Meyers ◽  
Seth R. Bordenstein
Keyword(s):  
Drosophila Melanogaster ◽  
Copy Number ◽  
Cytoplasmic Incompatibility ◽  
Functional Study ◽  
Content Type ◽  
Transgenic Expression ◽  
Additional Gene ◽  
Reproductive Parasitism ◽  
Transcript Length ◽  
Male Killing

ABSTRACT Endosymbiotic bacteria in the genus Wolbachia remarkably infect nearly half of all arthropod species. They spread in part because of manipulations of host sexual reproduction that enhance the maternal transmission of the bacteria, including male killing (death of infected males) and unidirectional cytoplasmic incompatibility (CI; death of offspring from infected fathers and uninfected mothers). Recent discoveries identified several genes in prophage WO of Wolbachia (wmk, cifA, and cifB) that fully or partially recapitulate male killing or CI when transgenically expressed in Drosophila melanogaster. However, it is not yet fully resolved if other gene candidates contribute to these phenotypes. Here, we transgenically tested 10 additional gene candidates for their involvement in male killing and/or CI. The results show that despite sequence and protein architecture similarities or comparative associations with reproductive parasitism, transgenic expression of the candidates does not recapitulate male killing or CI. Sequence analysis across Wmk and its closest relatives reveals amino acids that may be important to its function. In addition, evidence is presented to propose new hypotheses regarding the relationship between wmk transcript length and its ability to kill a given host, as well as copy number of wmk homologs within a bacterial strain, which may be predictive of host resistance. Together, these analyses continue to build the evidence for identification of wmk, cifA, and cifB as the major genes that have thus far been shown to cause reproductive parasitism in Wolbachia, and the transgenic resources provide a basis for further functional study of phage WO genes. IMPORTANCE Wolbachia are widespread bacterial endosymbionts that manipulate the reproduction of diverse arthropods to spread through a population and can substantially shape host evolution. Recently, reports identified three prophage WO genes (wmk, cifA, and cifB) that transgenically recapitulate many aspects of reproductive manipulation in Drosophila melanogaster. Here, we transgenically tested 10 additional gene candidates for CI and/or male killing in flies. The results yield no evidence for the involvement of these gene candidates in reproductive parasitism, bolstering the evidence for identification of the cif and wmk genes as the major factors involved in their phenotypes. In addition, evidence supports new hypotheses for prediction of male-killing phenotypes or lack thereof based on wmk transcript length and copy number. These experiments inform efforts to understand the full basis of reproductive parasitism for basic and applied purposes and lay the foundation for future work on the function of an interesting group of Wolbachia and phage WO genes.

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