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The discovery of two genes encoded by prophage WO from Wolbachia that functionally recapitulate and enhance cytoplasmic incompatibility in arthropods is the first inroad in solving the genetic basis of reproductive parasitism. Manipulation of insect survival by Wolbachia bacteria Bacteria from the genus Wolbachia infect many arthropods, including the mosquitoes that are vectors for many viruses that infect humans. Wolbachia infection causes 'cytoplasmic incompatibility', which means that crosses between infected males and uninfected females lead to embryonic death, increasing the proportion of infected females in the population. The molecular basis for this effect has been unknown. Here, Seth Bordenstein and colleagues use comparative and transgenic approaches to identify two genes encoded by the prophage WO from Wolbachia that recapitulate cytoplasmic incompatibility. The discovery of these cytoplasmic incompatibility factors could lead to the genetic manipulation of WO-induced reproductive alterations, and may feed into efforts to control the transmission of arthropod-borne viruses to humans. The genus Wolbachia is an archetype of maternally inherited intracellular bacteria that infect the germline of numerous invertebrate species worldwide. They can selfishly alter arthropod sex ratios and reproductive strategies to increase the proportion of the infected matriline in the population. The most common reproductive manipulation is cytoplasmic incompatibility, which results in embryonic lethality in crosses between infected males and uninfected females. Females infected with the same Wolbachia strain rescue this lethality. Despite more than 40 years of research 1 and relevance to symbiont-induced speciation 2 , 3 , as well as control of arbovirus vectors 4 , 5 , 6 and agricultural pests 7 , the bacterial genes underlying cytoplasmic incompatibility remain unknown. Here we use comparative and transgenic approaches to demonstrate that two differentially transcribed, co-diverging genes in the eukaryotic association module of prophage WO 8 from Wolbachia strain w Mel recapitulate and enhance cytoplasmic incompatibility. Dual expression in transgenic, uninfected males of Drosophila melanogaster crossed to uninfected females causes embryonic lethality. Each gene additively augments embryonic lethality in crosses between infected males and uninfected females. Lethality associates with embryonic defects that parallel those of wild-type cytoplasmic incompatibility and is notably rescued by w Mel-infected embryos in all cases. The discovery of cytoplasmic incompatibility factor genes cifA and cifB pioneers genetic studies of prophage WO-induced reproductive manipulations and informs the continuing use of Wolbachia to control dengue and Zika virus transmission to humans.

Animal hosts have initiated myriad symbiotic associations with microorganisms and often have maintained these symbioses for millions of years, spanning drastic changes in ecological conditions and lifestyles. The establishment and persistence of these relationships require genetic innovations on the parts of both symbionts and hosts. The nature of symbiont innovations depends on their genetic population structure, categorized here as open, closed or mixed. These categories reflect modes of inter-host transmission that result in distinct genomic features, or genomic syndromes, in symbionts. Although less studied, hosts also innovate in order to preserve and control symbiotic partnerships. New capabilities to sequence host-associated microbial communities and to experimentally manipulate both hosts and symbionts are providing unprecedented insights into how genetic innovations arise under different symbiont population structures and how these innovations function to support symbiotic relationships.The evolutionary persistence of animal symbioses depends on both host and symbiont innovations. Perreau and Moran review how genome sequencing and related experiments have clarified how these innovations arise under different symbiont population structures, categorized here as open, closed and mixed.

Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed γ-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the γ-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.

Aedes aegypti mosquitoes infected with the wMel strain of Wolbachia are being released into natural mosquito populations in the tropics as a way of reducing dengue transmission. High temperatures adversely affect wMel, reducing Wolbachia density and cytoplasmic incompatibility in some larval habitats that experience large temperature fluctuations. We monitored the impact of a 43.6°C heatwave on the wMel infection in a natural population in Cairns, Australia, where wMel was first released in 2011 and has persisted at a high frequency. Wolbachia infection frequencies in the month following the heatwave were reduced to 83% in larvae sampled directly from field habitats and 88% in eggs collected from ovitraps, but recovered to be near 100% four months later. Effects of the heatwave on wMel appeared to be stage-specific and delayed, with reduced frequencies and densities in field-collected larvae and adults reared from ovitraps but higher frequencies in field-collected adults. Laboratory experiments showed that the effects of heatwaves on cytoplasmic incompatibility and density are life stage-specific, with first instar larvae being the most vulnerable to temperature effects. Our results indicate that heatwaves in wMel-infected populations will have only temporary effects on Wolbachia frequencies and density once the infection has established in the population. Our results are relevant to ongoing releases of wMel-infected Ae. aegypti in several tropical countries.

The continuously high incidence of some endosymbionts in arthropods despite potential conflicts with their hosts is often explained by obligatory relationships, in which the host is fully dependent on its endosymbiont, fitness advantages conferred on hosts by facultative endosymbionts, or reproductive manipulation of hosts by endosymbionts (typically facultative). Yet continuously endosymbiont high incidence is sometimes observed without clear evidence supporting any of these mechanisms. This situation could potentially be explained by the presence of several coinfecting strains of the same endosymbiont species, each affecting the host differently such that their effects counteract one another when studied collectively. Here, we investigated Wolbachia endosymbionts of fleas, which stably persist in high loads in all females, with no indication that any of the above mechanisms explain their continuously high incidence. We sequenced fleas and identified two Wolbachia strains, designated as w Sc1 and w Sc2. We then correlated the strain composition in fleas with measures of their reproductive success. We found that fleas with high w Sc1 and low w Sc2 loads had a higher reproductive success than fleas that had high loads of both strains, low loads of both strains, or no Wolbachia , suggesting that w Sc1 may provide a direct fitness advantage to their hosts. Conversely, the number of males and total offspring was negatively correlated with w Sc2 levels, supporting male killing. Our research demonstrates that endosymbionts’ continuously high incidence may persist through intricate relationships in nature.

A naturally occurring Wolbachia strain (wAnga-Mali) was identified in mosquitoes of the Anopheles gambiae complex collected in the Malian villages of Dangassa and Kenieroba. Phylogenetic analysis of the nucleotide sequence of two 16S rRNA regions showed that wAnga-Mali clusters with Wolbachia strains from supergroup A and has the highest homology to a Wolbachia strain isolated from cat fleas (Ctenocephalides). wAnga-Mali is different from two Wolbachia strains previously reported in A. gambiae from Burkina Faso (wAnga_VK5_STP and wAnga_VK5_3.1a). Quantitative analysis of Wolbachia and Plasmodium sporozoite infection in field-collected mosquitoes indicates that the prevalence and intensity of Plasmodium falciparum sporozoite infection is significantly lower in Wolbachia-infected females. The presence of Wolbachia in females from a laboratory Anopheles coluzzii (A. gambiae, M form) colony experimentally infected with P. falciparum (NF54 strain) gametocyte cultures slightly enhanced oocyst infection. However, Wolbachia infection significantly reduced the prevalence and intensity of sporozoite infection, as observed in the field. This indicates that wAnga-Mali infection does not limit early stages of Plasmodium infection in the mosquito, but it has a strong deleterious effect on sporozoites and reduces malaria transmission.

Wolbachia used to counter dengue fever The mosquito-borne viral disease dengue fever is an increasing problem in tropical and subtropical regions. Traditional control measures aimed at reducing populations of the main transmission vector, Aedes aegypti , have had little success. Two papers in this issue report an alternative approach to mosquito population control using the bacterium Wolbachia pipientis , natural insect symbionts that facilitate their own transmission through a process called cytoplasmic incompatibility. In the first paper, Scott O'Neill and colleagues describe a Wolbachia strain derived from fruitflies that significantly reduces dengue virus carriage in mosquitoes without imposing a fitness cost. In the second paper, they demonstrate in a controlled field trial that the release of colonized mosquitoes leads to successful invasion of natural mosquito populations. These results suggest a viable strategy to control dengue fever. Dengue fever is the most important mosquito-borne viral disease of humans with more than 50 million cases estimated annually in more than 100 countries 1 , 2 . Disturbingly, the geographic range of dengue is currently expanding and the severity of outbreaks is increasing 2 , 3 , 4 . Control options for dengue are very limited and currently focus on reducing population abundance of the major mosquito vector, Aedes aegypti 5 , 6 . These strategies are failing to reduce dengue incidence in tropical communities and there is an urgent need for effective alternatives. It has been proposed that endosymbiotic bacterial Wolbachia infections of insects might be used in novel strategies for dengue control 7 , 8 , 9 . For example, the w MelPop-CLA Wolbachia strain reduces the lifespan of adult A. aegypti mosquitoes in stably transinfected lines 8 . This life-shortening phenotype was predicted to reduce the potential for dengue transmission. The recent discovery that several Wolbachia infections, including w MelPop-CLA, can also directly influence the susceptibility of insects to infection with a range of insect and human pathogens 9 , 10 , 11 has markedly changed the potential for Wolbachia infections to control human diseases. Here we describe the successful transinfection of A. aegypti with the avirulent w Mel strain of Wolbachia , which induces the reproductive phenotype cytoplasmic incompatibility with minimal apparent fitness costs and high maternal transmission, providing optimal phenotypic effects for invasion. Under semi-field conditions, the w Mel strain increased from an initial starting frequency of 0.65 to near fixation within a few generations, invading A. aegypti populations at an accelerated rate relative to trials with the w MelPop-CLA strain. We also show that w Mel and w MelPop-CLA strains block transmission of dengue serotype 2 (DENV-2) in A. aegypti , forming the basis of a practical approach to dengue suppression 12 .

Palm houses in Europe serve as urban biodiversity hot spots for alien spiders. As a result of several years of research in the Poznań Palm House, we documented the occurrence of 14 spider species, 9 of which were alien to Europe: Coleosoma floridanum , Hasarius adansoni , Howaia mogera , Ostearius melanopygius , Parasteatoda tabulata , Parasteatoda tepidariorum , Scytodes fusca , Spermophora kerinci and Triaeris stenaspis . The most abundant species was C. floridanum (39.9%). Three spider species were recorded for the first time in Poland: C. floridanum , S. fusca and S. kerinci . We studied the occurrence of endosymbiotic Wolbachia and Cardinium in parthenogenetic T. stenaspis and recorded for the first time the occurrence of Wolbachia in this spider. The endosymbiont was characterized based on the sequences of six bacterial housekeeping genes: 16S rRNA, coxA , fbpA , ftsZ , gatB and hcpA . Our phylogenetic reconstruction of Wolbachia supergroups revealed that the bacteria recovered from the spider formed distinct lineages in relation to all known supergroups. We assigned it to a novel supergroup X with unique sequences within the 16S rRNA and ftsZ genes. We discussed faunistic results in terms of long-term survival rates and the risk of invasion of alien species of spiders.

Background Psyllids (Hemiptera: Psylloidea) comprise a group of plant sap-sucking insects that includes important agricultural pests. They have close associations not only with plant pathogens, but also with various microbes, including obligate mutualists and facultative symbionts. Recent studies are revealing that interactions among such bacterial populations are important for psyllid biology and host plant pathology. In the present study, to obtain further insight into the ecological and evolutionary behaviors of bacteria in Psylloidea, we analyzed the microbiomes of 12 psyllid species belonging to the family Psyllidae (11 from Psyllinae and one from Macrocorsinae), using high-throughput amplicon sequencing of the 16S rRNA gene. Results The analysis showed that all 12 psyllids have the primary symbiont, Candidatus Carsonella ruddii (Gammaproteobacteria: Oceanospirillales), and at least one secondary symbiont. The majority of the secondary symbionts were gammaproteobacteria, especially those of the family Enterobacteriaceae (order: Enterobacteriales). Among them, symbionts belonging to “endosymbionts3”, which is a genus-level monophyletic group assigned by the SILVA rRNA database , were the most prevalent and were found in 9 of 11 Psyllinae species. Ca . Fukatsuia symbiotica and Serratia symbiotica , which were recognized only as secondary symbionts of aphids, were also identified. In addition to other Enterobacteriaceae bacteria, including Arsenophonus , Sodalis , and “endosymbionts2”, which is another genus-level clade, Pseudomonas (Pseudomonadales: Pseudomonadaceae) and Diplorickettsia (Diplorickettsiales: Diplorickettsiaceae) were identified. Regarding Alphaproteobacteria, the potential plant pathogen Ca . Liberibacter europaeus (Rhizobiales: Rhizobiaceae) was detected for the first time in Anomoneura mori (Psyllinae), a mulberry pest. Wolbachia (Rickettsiales: Anaplasmataceae) and Rickettsia (Rickettsiales: Rickettsiaceae), plausible host reproduction manipulators that are potential tools to control pest insects, were also detected. Conclusions The present study identified various bacterial symbionts including previously unexpected lineages in psyllids, suggesting considerable interspecific transfer of arthropod symbionts. The findings provide deeper insights into the evolution of interactions among insects, bacteria, and plants, which may be exploited to facilitate the control of pest psyllids in the future.

In the last decade, bacterial symbionts have been shown to play an important role in protecting hosts against pathogens. Wolbachia, a widespread symbiont in arthropods, can protect Drosophila and mosquito species against viral infections. We have investigated antiviral protection in 19 Wolbachia strains originating from 16 Drosophila species after transfer into the same genotype of Drosophila simulans. We found that approximately half of the strains protected against two RNA viruses. Given that 40% of terrestrial arthropod species are estimated to harbour Wolbachia, as many as a fifth of all arthropods species may benefit from Wolbachia-mediated protection. The level of protection against two distantly related RNA viruses--DCV and FHV--was strongly genetically correlated, which suggests that there is a single mechanism of protection with broad specificity. Furthermore, Wolbachia is making flies resistant to viruses, as increases in survival can be largely explained by reductions in viral titer. Variation in the level of antiviral protection provided by different Wolbachia strains is strongly genetically correlated to the density of the bacteria strains in host tissues. We found no support for two previously proposed mechanisms of Wolbachia-mediated protection--activation of the immune system and upregulation of the methyltransferase Dnmt2. The large variation in Wolbachia's antiviral properties highlights the need to carefully select Wolbachia strains introduced into mosquito populations to prevent the transmission of arboviruses.