The Genetics and Cell Biology of <i>Wolbachia</i>-Host Interactions

Serbus, Laura R.; Casper-Lindley, Catharina; Landmann, Frédéric; Sullivan, William

doi:10.1146/annurev.genet.41.110306.130354

Cited by 374 publications

(342 citation statements)

References 153 publications

(182 reference statements)

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“…It is important to note that although Buchnera are closely associated with the germline during development, they never invade the germline. This distinction is significant when considering transmission of the endosymbiont Wolbachia, which infects the germline of its host (56). Although the cell biology of Wolbachia host interactions is particularly well characterized and has benefitted from a lot of careful and elegant work in the model insect Drosophila (e.g., refs.…”

Section: Elucidating the Cellular And Developmental Mechanism Of Hostmentioning

confidence: 99%

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

Wilson

Duncan

2015

Proc. Natl. Acad. Sci. U.S.A.

123

102

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The role of symbiosis in bacterial symbiont genome evolution is well understood, yet the ways that symbiosis shapes host genomes or more particularly, host/symbiont genome coevolution in the holobiont is only now being revealed. Here, we identify three coevolutionary signatures that characterize holobiont genomes. The first signature, host/symbiont collaboration, arises when completion of essential pathways requires host/endosymbiont genome complementarity. Metabolic collaboration has evolved numerous times in the pathways of amino acid and vitamin biosynthesis. Here, we highlight collaboration in branched-chain amino acid and pantothenate (vitamin B5) biosynthesis. The second coevolutionary signature is acquisition, referring to the observation that holobiont genomes acquire novel genetic material through various means, including gene duplication, lateral gene transfer from bacteria that are not their current obligate symbionts, and full or partial endosymbiont replacement. The third signature, constraint, introduces the idea that holobiont genome evolution is constrained by the processes governing symbiont genome evolution. In addition, we propose that collaboration is constrained by the expression profile of the cell lineage from which endosymbiont-containing host cells, called bacteriocytes, are derived. In particular, we propose that such differences in bacteriocyte cell lineage may explain differences in patterns of host/endosymbiont metabolic collaboration between the sap-feeding suborders Sternorrhyncha and Auchenorrhynca. Finally, we review recent studies at the frontier of symbiosis research that are applying functional genomic approaches to characterization of the developmental and cellular mechanisms of host/endosymbiont integration, work that heralds a new era in symbiosis research.

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Section: Elucidating the Cellular And Developmental Mechanism Of Hostmentioning

confidence: 99%

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

Wilson

Duncan

2015

Proc. Natl. Acad. Sci. U.S.A.

123

102

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“…Despite CI's widespread occurrence, its molecular basis remains elusive (but see Serbus et al 2008 for reviews on this area). A useful conceptualization of the phenomenon is provided by the mod/resc (modification/rescue) model (Werren 1997).…”

Section: Introductionmentioning

confidence: 99%

On the Genetic Architecture of Cytoplasmic Incompatibility: Inference from Phenotypic Data

Nor¹,

Engelstädter²,

Duron³

et al. 2013

The American Naturalist

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. abstract: Numerous insects carry intracellular bacteria that manipulate the insects' reproduction and thus facilitate their own spread. Cytoplasmic incompatibility (CI) is a common form of such manipulation, where a (currently uncharacterized) bacterial modification of male sperm induces the early death of embryos unless the fertilized eggs carry the same bacteria, inherited from the mother. The death of uninfected embryos provides an indirect selective advantage to infected ones, thus enabling the spread of the bacteria. Here we use and expand recently developed algorithms to infer the genetic architecture underlying the complex incompatibility data from the mosquito Culex pipiens. We show that CI requires more genetic determinants than previously believed and that quantitative variation in gene products potentially contributes to the observed CI patterns. In line with population genetic theory of CI, our analysis suggests that toxin factors (those inducing embryo death) are present in fewer copies in the bacterial genomes than antitoxin factors (those ensuring that infected embryos survive). In combination with comparative genomics, our approach will provide helpful guidance to identify the genetic basis of CI and more generally of other toxin/antitoxin systems that can be conceptualized under the same framework.

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“…convergent evolution | metagenomics | nitrogen metabolism | eukaryotic-like proteins M icroorganisms form symbiotic relationships with eukaryotes encompassing all evolutionary stages, from simple amoebae to mammals. Symbiotic systems can range in complexity from those with a single dominant microorganism [e.g., Wolbachia in insects (1) or Vibrio in squids (2)] to those with hundreds of obligate or facultative microbial symbionts [e.g., communities in termite hindgut (3) or human colon (4)]. Mechanisms that shape the structure of complex symbiont communities are largely unknown (5); however, recent work on communities of free-living microorganisms indicates that both niche and neutral effects can play a role (6,7).…”

mentioning

confidence: 99%

Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts

Fan

Reynolds

Liu

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

329

464

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Microorganisms often form symbiotic relationships with eukaryotes, and the complexity of these relationships can range from those with one single dominant symbiont to associations with hundreds of symbiont species. Microbial symbionts occupying equivalent niches in different eukaryotic hosts may share functional aspects, and convergent genome evolution has been reported for simple symbiont systems in insects. However, for complex symbiont communities, it is largely unknown how prevalent functional equivalence is and whether equivalent functions are conducted by evolutionarily convergent mechanisms. Sponges represent an evolutionarily divergent group of species with common physiological and ecological traits. They also host complex communities of microbial symbionts and thus are the ideal model to test whether functional equivalence and evolutionary convergence exist in complex symbiont communities across phylogenetically divergent hosts. Here we use a sampling design to determine the phylogenetic and functional profiles of microbial communities associated with six sponge species. We identify common functions in the six microbiomes, demonstrating the existence of functional equivalence. These core functions are consistent with our current understanding of the biological and ecological roles of sponge-associated microorganisms and also provide insight into symbiont functions. Importantly, core functions also are provided in each sponge species by analogous enzymes and biosynthetic pathways. Moreover, the abundance of elements involved in horizontal gene transfer suggests their key roles in the genomic evolution of symbionts. Our data thus demonstrate evolutionary convergence in complex symbiont communities and reveal the details and mechanisms that underpin the process.

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The Genetics and Cell Biology of Wolbachia-Host Interactions

Cited by 374 publications

References 153 publications

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

On the Genetic Architecture of Cytoplasmic Incompatibility: Inference from Phenotypic Data

Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts

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