Wolbachia is a genus of gram-negative bacteria infecting many species of arthropods and filarial nematodes. The relationship between Wolbachia and its hosts ranges from parasitism through benign symbiosis up to obligate mutualism. It is one of the most common parasitic microbes of arthropods, and is possibly the most widespread reproductive parasite bacterium in the biosphere. Its interactions with hosts are complex and highly diverse across the various species in which it is found. Some host species cannot reproduce, or even survive, absent internal Wolbachia colonies. One study concluded that more than 16% of neotropical insect species carry bacteria of this genus, and as many as 25–70% of all insect species are estimated to be potential hosts.
History The first organism classified as Wolbachia was discovered in 1924 by Marshall Hertig and Simeon Burt Wolbach in the common house mosquito. They described it as "a somewhat pleomorphic, rodlike, gram-negative, intracellular organism [that] apparently infects only the ovaries and testes". Hertig formally described the species in 1936, and proposed both the generic and specific names: Wolbachia pipientis.
Research on Wolbachia intensified after 1971, when Janice Yen and A. Ralph Barr of UCLA discovered that Culex mosquito eggs were killed by a cytoplasmic incompatibility when the sperm of Wolbachia-infected males fertilized infection-free eggs.
Since, a large number of bacteria with close phylogenetic affinity to the originally detected W. pipientis have been discovered in a variety of hosts spanning over the Arthropoda and Nematoda phyla. The taxonomic classification of the various discovered groups remains a subject of debate, with no consensus on whether these groups of Wolbachia pipientis-like organisms should be categorized as the same or different species. Therefore, the strains are collectively referred to as Wolbachia, with the various groups of phylogenetically closely related strains designated as supergroups rather than distinct species. In general, each supergroup corresponds to a specific host or group of hosts. The genus Wolbachia is of considerable interest today due to its ubiquitous distribution, its many different evolutionary interactions, and its potential use as a biocontrol agent.
Phylogenetic studies have shown that the closest relatives to Wolbachia are the genera Francisella and Bartonella. Unlike Wolbachia, which needs a host cell to multiply, relatives belonging to these genera can be cultured on agar plates.
Method of sexual differentiation in hosts Wolbachia can infect many different types of organs, but are most notable for the infections of the testes and ovaries of their hosts altering the reproduction abilities of these. Wolbachia species are ubiquitous in mature eggs, but not mature sperm. Only infected females, therefore, pass the infection on to their offspring. Wolbachia bacteria maximize their spread by altering the reproductive capabilities of their hosts in such a way as to favour the infected females. Several different examples of this favoring have been observed, including:
Male killing, which occurs when infected males die during larval development, which increases the rate of born, infected females. Feminization, which results in infected males that develop as females or infertile pseudofemales. This is especially prevalent in Lepidoptera species such as the adzuki bean borer (Ostrinia scapulalis). Parthenogenesis, successful reproduction absent fertilization by the relevant male of the species. Some scientists have suggested that parthenogenesis may always be attributable to the effects of Wolbachia, though this is not the case for the marbled crayfish. An example of parthenogenesis induced by presence of Wolbachia are some species within the Trichogramma parasitoid wasp genus, which have evolved to procreate without males due to the presence of Wolbachia. Males are rare in this genus of wasp, possibly because many have been killed by that same strain of Wolbachia. Cytoplasmic incompatibility, the inability of Wolbachia-infected males to successfully reproduce with uninfected females or females infected with another Wolbachia strain. This reduces the reproductive success of those uninfected females and therefore promotes the infecting strain. In the cytoplasmic incompatibility mechanism, Wolbachia interferes with the parental chromosomes during the first mitotic divisions to the extent that they can no longer divide in synchrony.
Effects of sexual differentiation in hosts Several host species, such as those within the genus Trichogramma, are so dependent on sexual differentiation of Wolbachia that they are unable to reproduce effectively without the bacteria in their bodies, and some might even be unable to survive uninfected.
One study on infected woodlice showed the broods of infected organisms had a higher proportion of females than their uninfected counterparts. However, the broods also often consisted of fewer eggs than the broods of the uninfected Oniscus asellus.
Wolbachia, especially Wolbachia-caused cytoplasmic incompatibility, may be important in promoting speciation. Wolbachia strains that distort the sex ratio may alter their host's pattern of sexual selection in nature, and also engender strong selection to prevent their action, leading to some of the fastest examples of natural selection in natural populations.
The male killing and feminization effects of Wolbachia infections can also lead to speciation in their hosts. For example, populations of the pill woodlouse, Armadillidium vulgare which are exposed to the feminizing effects of Wolbachia, have been known to lose their female-determining chromosome. In these cases, only the presence of Wolbachia can cause an individual to develop into a female. Cryptic species of ground wētā (Hemiandrus maculifrons complex) are host to different lineages of Wolbachia which might explain their speciation without ecological or geographical separation.
Effect on aromatase
The enzyme aromatase is found to mediate sex-change in many species of fish. Wolbachia can affect the activity of aromatase in developing fish embryos.
Mechanism of host transfer
Step 1: Physical transfer
Predator-prey interactions Wolbachia may transfer from prey to predator through the digestive system. To do so, Wolbachia needs to first survive through the lumen secretion and then enter the host tissue through the gut epithelium. This route does not seem to occur frequently due to little evidence.
Host–parasitoid/parasite interactions This may be one of the most common routes of Wolbachia host shifts. Compared to predator-prey interactions, the physical association between the host and parasites typically lasts longer, occurs at various developmental stages, and enables Wolbachia to directly contact various tissues.
Since this interaction may expose both sides to microbial exchange, one strategy for understanding the direction of transfer is to assess Wolbachia's presence in close relatives on both sides, as the donor side generally has a larger diversity of infection.
One parasitoid species can infect multiple shared hosts, and one host species can infect multiple parasitoids. For instance, parthenogenesis-inducing Wolbachia can spread between Trichogramma parasitoid wasps sharing host eggs.
Parasites can also serve as a vector between infected and uninfected hosts without being infected. When the mouthparts and ovipositors of aphelinid parasitoid wasps become contaminated through feeding on Wolbachia-infected Bemisia tabaci, it can infect the next host.
Shared plant and other food sources This route applies to microbes that can survive either within or on the surface of the food. Experiments demonstrated that the Wolbachia wAlbB strain can survive extracellularly for up to 7 days, and up to 50 days for some strains in cotton leaf phloem vessels.
Plants are one of the best platforms for this route. By physical contact between arthropod mouthparts and plant tissue, the Wolbachia inhabiting the salivary glands of some insects may be transferred to the plants. As a result, arthropod species feeding on the same plants may share common Wolbachia strains.
Other insect food sources may also mediate Wolbachia horizontal transfer, such as the sharing of dung patches between two Malagasy dung beetle species.
Step 2: Survival and proliferation in the new host The pathogen-associated molecular patterns (PAMPs) in the bacteria, such as peptidoglycan, can activate the host's innate immune responses. In response, some Wolbachia strains have a unique functional peptidoglycan amidase (AmiDwol) that cleaves its bacterial cell wall so that it can escape from immune responses. Besides the peptidoglycans, cell-to-cell movements of Wolbachia can also cause oxidative stress to the host and trigger the host's immune response. Therefore, Wolbachia has a triple-layer vacuole that acts as a mechanical shield to protect it from cellular immune responses.
Step 3: Vertical transmission Vertical transmission requires Wolbachia to reach germ line cells and maintain in the zygote. Wolbachia may initially occupy somatic stem cells as a stable reservoir and then use the host's vitellogenin transovarial transportation system to enter the oocyte. Once Wolbachia enter the zygote, they need to reach important host tissues without disrupting the embryo's development. This can be achieved using the host cytoskeleton, by bundling Wolbachia protein WD0830 to host actin filaments. They can also increase the division rate of germ-line stem cells to localize and increase their titer. Under natural conditions, successful vertical transmission of Wolbachia is challenging.
Step 4: Spread within the host population Invasion of a new population likely stems from specific phenotypic effects, including reproductive manipulations and/or providing direct fitness benefits to their female hosts.
Upon transferring into a new host, Wolbachia may retain its original phenotypic effects, induce a different phenotype, or have no detectable effect. For instance, a strain that induces male killing in the moth Cadra cautella induced cytoplasmic incompatibility in a novel moth host Ephestia kuehniella.
Fitness advantages by Wolbachia infections Wolbachia infection has been linked to viral resistance in Drosophila melanogaster, Drosophila simulans, and mosquito species. Flies, including mosquitoes, infected with the bacteria are more resistant to positive-sense ssRNA viruses such as Drosophila C virus, norovirus, flock house virus, cricket paralysis virus, chikungunya virus, Zika virus, and West Nile virus.
In the common house mosquito, higher levels of Wolbachia were correlated with more insecticide resistance.
In leafminers of the species Phyllonorycter blancardella, Wolbachia bacteria help their hosts produce green islands on yellowing tree leaves, that is, small areas of leaf remaining fresh, allowing the larvae to continue feeding while growing to their adult forms. Larvae treated with tetracycline, which kills Wolbachia, lose this ability and subsequently only 13% emerge successfully as adult moths.
Muscidifurax uniraptor, a parasitoid wasp, also benefits from hosting Wolbachia bacteria.
In the parasitic filarial nematode species responsible for elephantiasis, such as Brugia malayi and Wuchereria bancrofti, Wolbachia has become an obligate endosymbiont and provides the host with chemicals necessary for its reproduction and survival. Elimination of the Wolbachia symbionts through antibiotic treatment therefore prevents reproduction of the nematode, and eventually results in its premature death.