Abstract
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.
Highlights
Phytophagous sap sucking insects in the insect order Hemiptera usually feed on nutritionally deficient xylem or phloem diets [1]
We aim to address the following questions: 1) What are the composition and diversity of bacterial communities in the bacteriomes and reproductive organs of these two cicada species? 2) Does H. cicadicola co-exist with S. muelleri in these two cicada species? 3) Do cicada species, sexes and tissues have any influence on the bacterial community composition and diversity? 4) What differences can be revealed between the bacterial communities investigated by using different research methods?
We further identified the unclassified operational taxonomic unit (OTU) by blasting their sequences with the GenBank database, and found that 90% of the unclassified OTUs are similar to H. cicadicola with an identity value of ~80%, which is the same as the sequence alignment results of the novel Rhizobiales bacterium (KR911840-KR911843) obtained by the Restriction Fragment Length Polymorphism (RFLP)
Summary
Phytophagous sap sucking insects in the insect order Hemiptera usually feed on nutritionally deficient xylem or phloem diets [1]. How do these insects survive with such a nutritionally poor diet? The most distinctive group is primary symbionts, such as Candidatus Buchnera aphidicola in aphids [4] and Candidatus Sulcia muelleri (hereafter Sulcia muelleri) in Auchenorrhyncha [5]. They are usually confined in the bacteriomes, specialized clusters of cells that house endosymbionts and protect them against the host immune system [6,7]. As a consequence of vertical transmission, primary symbionts co-evolve with their insect hosts [6,11,12,13,14,15]
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