Wolbachia: intracellular manipulators of mite reproduction

Cytoplasmically transmitted Wolbachia (alpha-Proteobacteria) are a group of closely related intracellular microorganisms that alter reproduction in arthropods. They are found in a few isopods and are widespread in insects. Wolbachia are implicated as the cause of parthenogenesis in parasitic wasps, feminization in isopods and reproductive (cytoplasmic) incompatibility in many insects. Here we report on the widespread occurrence of Wolbachia in spider mites and predatory mites based on a PCR assay for a 730 bp fragment of the ftsZ gene with primers that are specific for Wolbachia. An additional PCR, using two primer pairs that amplify a 259 bp region of the ftsZ gene that are diagnostic for the two Wolbachia subdivisions A and B, showed that infected mites only carried type B and not type A Wolbachia. The fact that some species tested negative for Wolbachia does not mean that the entire species is uninfected. We found that natural populations of Tetranychus urticae are polymorphic for the infection. The possible effects of Wolbachia on mite reproduction and post-zygotic reproductive isolation are discussed.To whom correspondence should be addressed at: Kruislaan 320, 1098 SM Amsterdam, The Netherlands     

Wolbachia: invasion biology in South pacific butterflies

Wolbachia ensdosymbionts are well known for their ability to manipulate the population biology and development of their hosts. One of the less studied outcomes of Wolbachia infection with this symbiont is the selective killing of male embryos. Recent work on butterflies living on different South Pacific islands is beginning to help us understand the complexity of the co-evolutionary interactions between these partners.     

Wolbachia genomes: revealing the biology of parasitism and mutualism

Wolbachia bacteria are endosymbiotic partners of many animal species, in which they behave as either parasites (in arthropod hosts) or mutualists (in nematode hosts). What biochemistry and biology underpin these diverse lifestyles? The recent complete sequencing of genomes from Wolbachia that infect the arthropod Drosophila melanogaster and the nematode Brugia malayi, together with the partial genome sequencing of three Wolbachia strains found in drosophilids, enables this question to begin to be addressed. Parasitic arthropod Wolbachia are characterized by the presence of phages that carry ankyrin-repeat proteins; these proteins might be exported to the host cell to manipulate reproduction. In nematode Wolbachia, which lack these phages, several biochemical pathways can deliver essential metabolites to the nematode hosts. Nematode Wolbachia might also have a role in modulating the mammalian host immune system but the sequenced Wolbachia genomes lack the genes to synthesize lipopolysaccharide, raising questions about the nature of the inducing molecule. The Wolbachia surface protein might carry out this function.     

Enterococcus infection biology: Lessons from invertebrate host models

The enterococci are commensals of the gastrointestinal tract of many metazoans, from insects to humans. While they normally do not cause disease in the intestine, they can become pathogenic when they infect sites outside of the gut. Recently, the enterococci have become important nosocomial pathogens, with the majority of human enterococcal infections caused by two species, Enterococcus faecalis and Enterococcus faecium. Studies using invertebrate infection models have revealed insights into the biology of enterococcal infections, as well as general principles underlying host innate immune defense. This review highlights recent findings on Enterococcus infection biology from two invertebrate infection models, the greater wax moth Galleria mellonella and the free-living bacteriovorous nematode Caenorhabditis elegans.     

Molecular biology of the invertebrate dopamine receptors

Dopamine is found in the nervous systems of both vertebrates and invertebrates. However, the specific actions of dopamine depend on the dopamine receptor type that is expressed in the target cell. As in mammals, different subtypes of dopamine receptors have been cloned and characterized from invertebrates, and these receptor subtypes have different structural and functional properties. Understanding how these receptors respond to dopamine and in which cells each receptor type is expressed is key to our understanding of the role of dopamine signaling. Comparison of the amino acid sequences and experimentally determined functional properties suggest that there are at least three distinct types of dopamine receptors in invertebrates. This review focuses on invertebrate dopamine receptors for which the genes have been isolated and identified, and examines our current knowledge of the functional and structural properties of these receptors, and their pharmacology and expression.     

The contribution of invertebrate study to the biology of nitric oxide

After the identification of nitric oxide (NO) with the endothelium derived-relaxing factor, many signaling mechanisms involving NO were identified through experiments on Mammals. NO activates soluble guanylyl cyclase leading to the formation of cGMP, stimulates the ADP-ribosylation of GAPDH, altering the cell energy production and combines with superoxide, generating cytotoxic peroxynitrite. NO was then progressively established as a major messenger molecule in Mammals. It is implied in the regulation of blood vessel dilatation, immune function, development and neurotransmission in brain and peripheral nervous system. Later, parallel findings were observed in Invertebrates and then, NO appeared as a signaling molecule widely spread throughout the animal kingdom and whose functions were highly conserved during evolution. The purpose of this short review is to highlight the contribution of Invertebrate studies to the knowledge of NO biology.     

Comparative biology of cAMP-induced germinal vesicle breakdown in marine invertebrate oocytes

During maturation, oocytes must undergo a process of nuclear disassembly, or "germinal vesicle breakdown" (GVBD), that is regulated by signaling pathways involving cyclic AMP (cAMP). In vertebrate and starfish oocytes, cAMP elevation typically prevents GVBD. Alternatively, increased concentrations of intra-oocytic cAMP trigger, rather than inhibit, GVBD in several groups of marine invertebrates. To integrate what is known about the stimulation of GVBD by intra-oocytic cAMP, this article reviews published data for ascidian, bivalve, brittle star, jellyfish, and nemertean oocytes. The bulk of the review concentrates on the three most intensively analyzed groups known to display cAMP-induced GVBD-nemerteans, ascidians, and jellyfish. In addition, this synopsis also presents some previously unpublished findings regarding the stimulatory effects of intra-oocytic cAMP on GVBD in jellyfish and the annelid worm Pseudopotamilla occelata. Finally, factors that may account for the currently known distribution of cAMP-induced GVBD across animal groups are discussed.     

Reproductive biology of the German cockroach,Blattella germanica: Juvenile hormone as a pleiotropic master regulator

Juvenile hormone (JH) exerts major pleiotropic effects on cockroach development and reproduction. The production of JH by the corpora allata (CA) in the adult female German cockroach, Blattella germanica, is dependent upon and modulated by both internal and environmental stimuli. Mating, intake of high-quality food, social interactions, and the presence of vitellogenic ovaries facilitate JH synthesis. Conversely, starvation, deficient diets, enforced virginity, isolation, and a pre- or post-vitellogenic ovary cause the CA to produce less JH. Sensory stimulation of the genital vestibulum by the ootheca also inhibits the CA via signals that ascend the ventral nerve cord. All these stimulatory and inhibitory signals are integrated by the brain, and a preponderance of favorable signals results in a graded lifting of brain inhibition, permitting the synthesis and release of JH. The effects of inhibitory signals on JH biosynthesis can be lifted experimentally by severing nervous connections between the brain and the CA. Such an operation accelerates activation of the CA. Besides controlling gonadal maturation in females, JH concurrently regulates the production of sexual signals, including both attractant- and courtship-eliciting pheromones, and the behavioral expression of calling (pheromone release) and sexual receptivity. Although JH is required for the expression of copulatory readiness in female B. germanica, it appears that signals associated with copulation (spermatophore, sperm, accessory secretions) can inhibit this behavioral state even when titers of JH are permissive for receptivity. These observations suggest that JH might regulate sexual receptivity in females indirectly through other directives. In males, JH accelerates not only the onset of sexual readiness but also synthesis of accessory reproductive products. Lastly, we present a novel cockroach control strategy that is based on the intimate association between food intake and rising JH titers in B. germanica females. JH analogs cause abortion of fertile oothecae in gravid females. In turn, rising JH titers and vitellogenic oocytes induce feeding in females. With strategic placement of insecticidal baits and JH analogs, gravid females, which normally feed little and are difficult to control, can thus be effectively targeted for elimination. Arch. Insect Biochem. Physiol. 35:405–426, 1997. © 1997 Wiley-Liss, Inc.     

Toward a Wolbachia Multilocus Sequence Typing System: Discrimination of Wolbachia Strains Present in Drosophila Species

Among the diverse maternally inherited symbionts in arthropods, Wolbachia are the most common and infect over 20% of all species. In a departure from traditional genotyping or phylogenetic methods relying on single Wolbachia genes, the present study represents an initial Multilocus Sequence Typing (MLST) analysis to discriminate closely related Wolbachia pipientis strains, and additional data on sequence diversity in Wolbachia. We report a new phylogenetic characterization of four genes (aspC, atpD, sucB, and pdhB), and provide an expanded analysis of markers described in previous studies (16S rDNA, ftsZ, groEL, dnaA, and gltA). MLST analysis of the bacterial strains present in 16 different Drosophila–Wolbachia associations detected four distinct clonal complexes that also corresponded to maximum-likelihood identified phylogenetic clades. Among the 16 associations analyzed, six could not be assigned to MLST clonal complexes and were also shown to be in conflict with relationships predicted by maximum-likelihood phylogenetic inferences. The results demonstrate the discriminatory power of MLST for identifying strains and clonal lineages of Wolbachia and provide a robust foundation for studying the ecology and evolution of this widespread endosymbiont.     

Stochastic spread of Wolbachia

Wolbachia are very common, maternally transmitted endosymbionts of insects. They often spread by a mechanism termed cytoplasmic incompatibility (CI) that involves reduced egg hatch when Wolbachia-free ova are fertilized by sperm from Wolbachia-infected males. Because the progeny of Wolbachia-infected females generally do not suffer CI-induced mortality, infected females are often at a reproductive advantage in polymorphic populations. Deterministic models show that Wolbachia that impose no costs on their hosts and have perfect maternal transmission will spread from arbitrarily low frequencies (though initially very slowly); otherwise, there will be a threshold frequency below which Wolbachia frequencies decline to extinction and above which they increase to fixation or a high stable equilibrium. Stochastic theory was used to calculate the probability of fixation in populations of different size for arbitrary current frequencies of Wolbachia, with special attention paid to the case of spread after the arrival of a single infected female. Exact results are given based on a Moran process that assumes a specific demographic model, and approximate results are obtained using the more general Wright-Fisher theory. A new analytical approximation for the probability of fixation is derived, which performs well for small population sizes. The significance of stochastic effects in the natural spread of Wolbachia and their relevance to the use of Wolbachia as a drive mechanism in vector and pest management are discussed.     

DNA manipulators: caught in the act

DNA is a dynamic molecule that undergoes constant changes in the cell through interactions with numerous proteins. Several classes of enzyme are specialized in promoting DNA rearrangements, including site-specific recombinases, DNA helicases, transposases and DNA topoisomerases. Recent structures of protein-DNA reaction intermediates trapped in various states of DNA remodeling, complemented by biochemical and biophysical functional studies, have enhanced our understanding of their respective mechanistic pathways.     

Wolbachia detection: an assessment of standard PCR protocols

Wolbachia is a large monophyletic genus of intracellular bacteria, traditionally detected using PCR assays. Its considerable phylogenetic diversity and impact on arthropods and nematodes make it urgent to assess the efficiency of these screening protocols. The sensitivity and range of commonly used PCR primers and of a new set of 16S primers were evaluated on a wide range of hosts and Wolbachia strains. We show that certain primer sets are significantly more efficient than others but that no single protocol can ensure the specific detection of all known Wolbachia infections.     

Infection by Wolbachia: from passengers to residents

Wolbachia are endosymbiotic alpha-proteobacteria harboured by terrestrial arthropods and filarial nematodes, where they are maternally transmitted through egg cytoplasm. According to the host group, Wolbachia have developed two contrasting symbiotic strategies. In arthropods, symbiosis is secondary (i.e. facultative), and Wolbachia insure their transmission as reproduction parasites. However, despite of the efficiency of the manipulation mechanisms used, Wolbachia are limited to the state of passenger because some factors can prevent the association between Wolbachia and their hosts to become permanent. On the contrary, symbiosis is primary (i.e. obligatory) in filarial nematodes where Wolbachia insure their transmission via a mutualistic relationship, leading them to become permanent residents of their hosts. However, a few examples show that in arthropods too some Wolbachia have started to present the first stages of a mutualistic behaviour, or are even truly indispensable to their host. Whatever its strategy, Wolbachia infection is a spectacular evolutionary success, this symbiotic bacterium representing one of the most important biomass of its kind. To cite this article: H. Merçot, D. Poinsot, C. R. Biologies 332 (2009).     

Wolbachia: Evolutionary novelty in a rickettsial bacteria

Background  

Although closely related, the alpha-proteobacteria Wolbachia and the Rickettsiacae (Rickettsia and Ehrlichia), employ different evolutionary life history strategies. Wolbachia are obligate endocellular symbionts that infect an extraordinary host range and, in contrast to the infectious and pathogenic Rickettsia and Ehrlichia, profoundly influence host reproductive biology.     

Wolbachia genomes: insights into an intracellular lifestyle

The genome sequence of the Wolbachia endosymbiont that infects the nematode Brugia malayi has recently been determined together with three partial Wolbachia genomes from different Drosophila species. These data along with the previously published Wolbachia genome from Drosophila melanogaster provide new insights into how this endosymbiont has managed to become so successful.     

Evolutionary consequences of Wolbachia infections

The past decade has revealed the bacterium Wolbachia as the most widespread symbiont of arthropods and nematodes. Behind this evolutionary success is an remarkable variety of effects on host biology, ranging from manipulation of reproduction in favor of females to more classical mutualistic interactions. Here we discuss the potential of Wolbachia for promoting evolutionary changes in its hosts.