Dataset Information

Analysis of Inter-Individual Bacterial Variation in Gut of Cicada Meimuna mongolica (Hemiptera: Cicadidae).

ABSTRACT: Intestinal bacterial community plays a crucial role in the nutrition, development, survival, and reproduction of insects. When compared with other insects with piercing-sucking mouthparts, the habitats of cicada nymphs and adults are totally different. However, little is known about the differences in the gut bacterial communities in the nymphs and adults within any cicada species. The diversity of bacteria in the gut of nymphs and adults of both genders of Meimuna mongolica (Distant) was studied using the denaturing gradient gel electrophoresis (DGGE) method. Few inter-individual variations among gut microbiota were observed, suggesting that M. mongolica typically harbors a limited and consistent suite of bacterial species. Bacteria in the genera Pseudomonas and Enterobacter were the predominant components of the gut microflora of M. mongolica at all life stages. Bacteria of Pantoea, Streptococcus, and Uruburuella were also widespread in the cicada samples but at relatively lower concentrations. The relative stability and similarity of the PCR-DGGE patterns indicate that all individuals of this cicada species harbor a characteristic bacterial community which is independent from developmental stages and genders. Related endosymbionts that could be harbored in bacteromes of cicadas were not detected in any gut samples, which could be related to the cicada species and the distribution of these endosymbionts in the cicada cavity, or due to some of the possible limitations of PCR-DGGE community profiling. It is worthwhile to further address if related cicada endosymbiont clades distribute in the alimentary canals and other internal organs through diagnostic PCR using group-specific primer sets.

SUBMITTER: Zhou W

PROVIDER: S-EPMC4626675 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Publications

Analysis of Inter-Individual Bacterial Variation in Gut of Cicada Meimuna mongolica (Hemiptera: Cicadidae).

Zhou Wenting W Nan Xiaoning X Zheng Zhou Z Wei Cong C He Hong H

Journal of insect science (Online) 20150927

Intestinal bacterial community plays a crucial role in the nutrition, development, survival, and reproduction of insects. When compared with other insects with piercing-sucking mouthparts, the habitats of cicada nymphs and adults are totally different. However, little is known about the differences in the gut bacterial communities in the nymphs and adults within any cicada species. The diversity of bacteria in the gut of nymphs and adults of both genders of Meimuna mongolica (Distant) was studie ...[more]

PMID: 26411784

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Project description:Cicadas form intimate symbioses with bacteria to obtain nutrients that are scarce in the xylem fluid they feed on. The obligate symbionts in cicadas are purportedly confined to specialized bacteriomes, but knowledge of bacterial communities associated with cicadas is limited. Bacterial communities in the bacteriomes and organs of reproductive, digestive and excretory systems of two cicada species (Platypleura kaempferi and Meimuna mongolica) were investigated using different methods, and the bacterial diversity and distribution patterns of dominant bacteria in different tissues were compared. Within each species, the bacterial communities of testes are significantly different from those of bacteriomes and ovaries. The dominant endosymbiont Candidatus Sulcia muelleri is found not only in the bacteriomes and reproductive organs, but also in the "filter chamber + conical segment" of both species. The transmission mode of this endosymbiont in the alimentary canal and its effect on physiological processes merits further study. A novel bacterium of Rhizobiales, showing ~80% similarity to Candidatus Hodgkinia cicadicola, is dominant in the bacteriomes and ovaries of P. kaempferi. Given that the genome of H. cicadicola exhibits rapid sequence evolution, it is possible that this novel bacterium is a related endosymbiont with beneficial trophic functions similar to that of H. cicadicola in some other cicadas. Failure to detect H. cicadicola in M. mongolica suggests that it has been subsequently replaced by another bacterium, a yeast or gut microbiota which compensates for the loss of H. cicadicola. The distribution of this novel Rhizobiales species in other cicadas and its identification require further investigation to help establish the definition of the bacterial genus Candidatus Hodgkinia and to provide more information on sequence divergence of related endosymbionts of cicadas. Our results highlight the complex bacterial communities of cicadas, and are informative for further studies of the interactions and co-evolution of insect-microbial symbioses in Cicadoidea.

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.

Dataset Information

Analysis of Inter-Individual Bacterial Variation in Gut of Cicada Meimuna mongolica (Hemiptera: Cicadidae).

Publications

Analysis of Inter-Individual Bacterial Variation in Gut of Cicada Meimuna mongolica (Hemiptera: Cicadidae).

Similar Datasets

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