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Interaction of viral pathogen with porin channels on the outer membrane of insect bacterial symbionts mediates their joint transovarial transmission.

ABSTRACT: Many hemipteran insects that can transmit plant viruses in a persistent and transovarial manner are generally associated with a common obligate bacterial symbiont Sulcia and its β-proteobacterial partner. Rice dwarf virus (RDV), a plant reovirus, can bind to the envelope of Sulcia through direct interaction of the viral minor outer capsid protein P2 with the bacterial outer membrane protein, allowing the virus to exploit the ancient oocyte entry path of Sulcia in rice leafhopper vectors. Here, we show that RDV can hitchhike with both Sulcia and its β-proteobacterial partner Nasuia to ensure their simultaneous transovarial transmission. Interestingly, RDV can move through the outer envelope of Nasuia and reside in the periplasmic space, which is mediated by the specific interaction of the viral major outer capsid protein P8 and the porin channel on the bacterial outer envelope. Nasuia porin-specific antibody efficiently interferes with the binding between RDV and the Nasuia envelope, thus strongly preventing viral transmission to insect offspring. Thus, RDV has evolved different strategies to exploit the ancient oocyte entry paths used by two obligate bacterial symbionts in rice leafhoppers. Our results thus reveal that RDV has formed complex, cooperative interactions with both Sulcia and Nasuia during their joint transovarial transmission. This article is part of the theme issue 'Biotic signalling sheds light on smart pest management'.

SUBMITTER: Wu W

PROVIDER: S-EPMC6367154 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Interaction of viral pathogen with porin channels on the outer membrane of insect bacterial symbionts mediates their joint transovarial transmission.

Wu Wei W Huang Lingzhi L Mao Qianzhuo Q Wei Jing J Li Jiajia J Zhao Yu Y Zhang Qian Q Jia Dongsheng D Wei Taiyun T

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20190301 1767

Many hemipteran insects that can transmit plant viruses in a persistent and transovarial manner are generally associated with a common obligate bacterial symbiont Sulcia and its β-proteobacterial partner. Rice dwarf virus (RDV), a plant reovirus, can bind to the envelope of Sulcia through direct interaction of the viral minor outer capsid protein P2 with the bacterial outer membrane protein, allowing the virus to exploit the ancient oocyte entry path of Sulcia in rice leafhopper vectors. Here, w ...[more]

PMID: 30967020

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Project description:Although transovarial transmission of bacteriome-associated symbionts in hemipteran insects is extremely important for maintaining intimate host-symbiont associations, our knowledge of cellular mechanisms underlying the transmission process is quite limited. We investigated bacterial communities of salivary glands, bacteriomes, and digestive and reproductive organs and clarified the transovarial transmission of bacteriome-associated symbionts of the mountain-habitat specialist Pycna repanda using integrated methods. The bacterial communities among different gut tissues and those of bacteriomes of males and females both show similarity, whereas differences are exhibited among bacterial communities in testes and ovaries. The primary symbionts "Candidatus Sulcia muelleri" (hereafter "Ca Sulcia") and "Candidatus Hodgkinia cicadicola" (hereafter "Ca Hodgkinia") were not only restricted to but also dominant in the bacteriomes and ovaries. "Ca Hodgkinia" cells in the bacteriomes of both sexes exhibited different colors by histological and electron microscopy. Also considering the results of a restriction fragment length polymorphism (RFLP)-based cloning approach, we hypothesize that "Ca Hodgkinia" may have split into cytologically different cellular lineages within this cicada species. Regarding the dominant secondary symbionts, Rickettsia was detected in the salivary glands, digestive organs, and testes, whereas Arsenophonus was detected in the bacteriomes and ovaries. Our results show that Arsenophonus can coexist with "Ca Sulcia" and "Ca Hodgkinia" within bacteriomes and can be transovarially transmitted with these obligate symbionts together from mother to offspring in cicadas, but it is not harbored in the cytoplasm of "Ca Sulcia." The change in the shape of "Ca Sulcia" and "Ca Hodgkinia" during the transovarial transmission process is hypothesized to be related to the limited space and novel microenvironment.IMPORTANCE Cicadas establish an intimate symbiosis with microorganisms to obtain essential nutrients that are extremely deficient in host plant sap. Previous studies on bacterial communities of cicadas mainly focused on a few widely distributed species, but knowledge about mountain-habitat species is quite poor. We initially revealed the physical distribution of the primary symbionts "Ca Sulcia" and "Ca Hodgkinia" and the dominant secondary symbionts Rickettsia and Arsenophonus in the mountain-habitat specialist Pycna repanda and then clarified the transovarial transmission process of bacteriome-associated symbionts in this species. Our observations suggest that "Ca Hodgkinia" may have split into cytologically distinct lineages within this cicada species, and related cicadas might have developed complex mechanisms for the vertical transmission of the bacteriome-associated symbionts. We also revealed that Arsenophonus can be transovarially transmitted in auchenorrhynchan insects when it is not harbored in the cytoplasm of other endosymbionts. Our results highlight transovarial transmission mechanisms of bacteriome-associated symbionts in sap-feeding insects.

Project description:The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Liviidae) is a serious pest worldwide, transmitting Candidatus Liberibacter spp. (Alphaproteobacteria), the causative agents of a devastating citrus disease known as huanglongbing or greening disease. In a symbiotic organ called the bacteriome, D. citri possesses an organelle-like defensive symbiont, Candidatus Profftella armatura (Betaproteobacteria), and a nutritional symbiont, Ca. Carsonella ruddii (Gammaproteobacteria). Drastically reduced symbiont genomes and metabolic complementarity among the symbionts and D. citri indicate their mutually indispensable association. Moreover, horizontal gene transfer between the Profftella and Liberibacter lineages suggests ecological and evolutionary interactions between the bacteriome symbiont and the HLB pathogen. Using fluorescence in situ hybridization, we examined the behavior of Profftella and Carsonella during transovarial transmission and the development of D. citri. In the bacteriomes of sexually-mature female adults, symbionts transformed from an extremely elongated tubular form into spherical or short-rod forms, which migrated toward the ovary. The symbionts then formed mosaic masses, which entered at the posterior pole of the vitellogenic oocytes. After anatrepsis, Carsonella and Profftella migrated to the central and peripheral parts of the mass, respectively. Following the appearance of host nuclei, the mass cellularized, segregating Carsonella and Profftella in the central syncytium and peripheral uninucleate bacteriocytes, respectively. Subsequently, the uninucleate bacteriocytes harboring Profftella assembled at the posterior pole, while the syncytium, containing Carsonella, sat on the anterior side facing the germ band initiating katatrepsis. During dorsal closure, the syncytium was divided into uninuclear bacteriocytes, which surrounded the mass of bacteriocytes containing Profftella. Once fully surrounded, the bacteriocyte mass containing Profftella was fused into a syncytium. Prior to hatching, a pair of wing-like protrusions arose from both lateral sides of the bacteriome, which continued to grow throughout the nymphal stages. These findings provide a foundation for better understanding the intricate relationship between D. citri and its microbiota.

Project description:BackgroundVector-borne pathogens must overcome arthropod infection and escape barriers (e.g. midgut and salivary glands) during the extrinsic incubation period (EIP) before subsequent transmission to another host. This particular timespan is undetermined for the etiological agent of flea-borne spotted fever (Rickettsia felis). Artificial acquisition of R. felis by blood-feeding cat fleas revealed dissemination to the salivary glands after seven days; however, this length of time is inconsistent with co-feeding studies that produced infectious cat fleas within 24 h of infection. In the current study, we demonstrated that an alternative mechanism is responsible for the early-phase transmission that typifies flea-borne R. felis spread.MethodsCo-feeding transmission bioassays were constructed to assess temporal dynamics of R. felis amongst cat fleas, including exposure time to produce infectious fleas and association time to transmit infection to naïve fleas. Additional experiments examined the proportion of R. felis-exposed cat fleas with contaminated mouthparts, as well as the likelihood for cat fleas to release R. felis from their mouthparts following exposure to an infectious bloodmeal. The potential for mechanical transmission of R. felis by co-feeding cat fleas was further examined using fluorescent latex beads, as opposed to a live pathogen, which would not require a biological mechanism to achieve transmission.ResultsAnalyses revealed that R. felis-infected cat fleas were infectious to naïve fleas less than 24 h after exposure to the pathogen, but showed no rickettsial dissemination to the salivary glands during this early-phase transmission. Additionally, the current study revealed that R. felis-infected cat fleas must co-feed with naïve fleas for more than 12 h in order for early-phase transmission to occur. Further evidence supported that contaminated flea mouthparts may be the source of the bacteria transmitted early, and demonstrated that R. felis is released from the mouthparts during brief probing events. Moreover, the use of fluorescent latex beads supports the notion that early-phase transmission of R. felis is a mechanical mechanism.ConclusionsDetermination of the transmission mechanisms utilized by R. felis is essential to fully understand the vulnerability of susceptible vertebrate hosts, including humans, to this pathogen.

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Interaction of viral pathogen with porin channels on the outer membrane of insect bacterial symbionts mediates their joint transovarial transmission.

Publications

Interaction of viral pathogen with porin channels on the outer membrane of insect bacterial symbionts mediates their joint transovarial transmission.

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