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Wolbachia: master manipulators of invertebrate biology

Key Points

  • This Review focuses on intracellular Wolbachia, which are globally widespread Rickettsia-like bacteria that infect many arthropod species, as well as filarial nematodes.

  • The authors discuss recent advances in Wolbachia research, with an emphasis on genetics and genomics, ecology, evolution and applications to pest and disease control.

  • Wolbachia are primarily reproductive parasites that have several different effects on hosts, including feminization, induced parthenogenesis, male killing and a sperm–egg incompatibility that is known as cytoplasmic incompatibility. Wolbachia can effectively manipulate the biology of host cells, and have evolved mutualisms with their hosts. These and other effects of Wolbachia are discussed, as well as recent advances on the understanding of cytological interactions between bacteria and their host.

  • Maintenance of the global Wolbachia pandemic is discussed, including factors that affect the spread of Wolbachia, transfer between host species and persistence within a host lineage. The usefulness of multilocus strain typing to characterize the movement and diversity of these bacteria is also emphasized.

  • The evolutionary implications of Wolbachia infection are discussed, including the possible role of this endosymbiont in the promotion of reproductive isolation and speciation, as well as its potential to contribute to host genome evolution through horizontal transfer of genes from the bacteria into their host.

  • Finally, the authors outline possible practical applications of Wolbachia in pest and disease vector management strategies and highlight the main unanswered questions regarding Wolbachia biology.

Abstract

Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm–egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.

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Figure 1: Phylogeny of Wolbachia.
Figure 2: Wolbachia-induced phenotypes.
Figure 3: The cytological basis of Wolbachia-induced cytoplasmic incompatibility.
Figure 4: Wolbachia-to-host lateral gene transfer in Drosophila ananassae.

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DATABASES

Entrez Genome Project

Brugia malayi

Drosophila ananassae

Drosophila melanogaster

Drosophila simulans

Legionella pneumophila

Orientia tsutsugamushi

Rickettsia bellii

FURTHER INFORMATION

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Anti-Wolbachia Project

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Wolbachia MLST databases

Glossary

Mutualism

A symbiotic relationship in which both partners benefit.

Commensalism

A symbiotic relationship in which neither partner benefits or is harmed.

Parasitism

A symbiotic relationship in which one partner benefits at the expense of the other.

Clade

A group of genetically related organisms that includes an ancestor and all of its descendants.

Meta-analysis

A method for combining results from separate, related studies.

Feminization

A process in which a male acquires female characteristics.

Haplodiploid

A sex-determining mechanism that is found in some insect groups, in which males are haploid and females are diploid.

Parthenogenesis

An asexual form of reproduction that is found in females, in which growth and development of embryos occurs without fertilization by males.

Heterogamety

The production of dissimilar gametes by an individual of one sex. For example, the production of X- and Y-bearing gametes by the human male.

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Werren, J., Baldo, L. & Clark, M. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6, 741–751 (2008). https://doi.org/10.1038/nrmicro1969

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