Dual “Bacterial-Fungal” Symbiosis in Deltocephalinae Leafhoppers (Insecta, Hemiptera, Cicadomorpha: Cicadellidae)

Abstract

The symbiotic systems (types of symbionts, their distribution in the host insect body, and their transovarial transmission between generations) of four Deltocephalinae leafhoppers: Fieberiella septentrionalis, Graphocraerus ventralis, Orientus ishidae, and Cicadula quadrinotata have been examined by means of histological, ultrastructural, and molecular techniques. In all four species, two types of symbionts are present: bacterium Sulcia (phylum Bacteroidetes) and yeast-like symbionts closely related to the entomopathogenic fungi (phylum Ascomycota, class Sordariomycetes). Sulcia bacteria are always harbored in giant bacteriocytes, which are grouped into large organs termed Bbacteriomes.^In F. septentrionalis, G. ventralis, and O. ishidae, numerous yeast-like microorganisms are localized in cells of the fat body, whereas in C. quadrinotata, they occupy the cells of midgut epithelium in large number. Additionally, in C. quadrinotata, a small amount of yeast-like microorganisms occurs intracellularly in the fat body cells and, extracellularly, in the hemolymph. Sulcia bacteria in F. septentrionalis, G. ventralis, O. ishidae, and C. quadrinotata, and the yeastlike symbionts residing in the fat body of F. septentrionalis, G. ventralis, and O. ishidae are transovarially transmitted; i.e., they infect the ovarioles which constitute the ovaries.

Recurrent symbiont recruitment from fungal parasites in cicadas

“…In the classic extensive histological surveys by German microbiologists ( 1 , 44 , 45 , 89 , 90 ), a comprehensive study detected fungal symbionts in as many as 237 (64%) of 370 species of plant-sucking hemipteran insects representing the Auchenorrhyncha (cicadas, spittlebugs, leafhoppers, treehoppers, planthoppers, etc.) ( 44 ), and recent studies, including this study, have shown that some of them are Ophiocordyceps -allied fungal symbionts ( 33 , 35 , 37 – 39 , 67 , 70 ). Here, we point out that such dynamic symbiont recruitment from fungal parasites may be taking place in diverse insects more generally than previously envisaged.…”

“…Mycologists have described Ophiocordyceps and allied fungi as insect parasites, including many cicada-parasitizing species ( 56 , 93 – 96 ). Recent molecular phylogenetic approaches have identified some of the yeast-like fungal symbionts of insects as close relatives of the Ophiocordyceps entomopathogens ( 25 , 33 , 35 , 37 – 39 , 65 – 70 ). Recent genomic approaches to the insect-associated microbial communities have uncovered many striking cases of drastic size reduction and extreme metabolic streamlining in ancient bacterial symbiont genomes, some of which look like they are almost going beyond the limit of being able to sustain basic cellular functioning ( 19 – 22 ).…”

“…By accumulating numerous mutations that could potentially lead to genomic malfunctioning and instability, such tiny-genome symbionts, and potentially their hosts, may be near the edge of extinction due to genome erosion ( 14 , 15 ). There are many examples, however, as in aphids ( 23 – 28 ), scale insects ( 29 , 30 ), spittlebugs ( 31 , 32 ), leafhoppers ( 33 – 37 ), planthoppers ( 38 , 39 ), weevils ( 40 , 41 ), lice ( 42 , 43 ), and others ( 1 , 44 , 45 ), wherein an ancient and presumably degraded bacterial symbiont with essential biological function has been lost and replaced by totally different microbial associates. Whether the degenerative trend of symbiont genome evolution is relevant to the symbiont losses, replacements, and diversification, and if so, how, is mostly unanswered but remains an intriguing issue of evolutionary biology.…”

Fungicides Reduce the Abundance of Yeast-like Symbionts and Survival of White-Backed Planthopper Sogatella furcifera (Homoptera: Delphacidae)

“…Similar to other rice planthoppers, the WBPH harbors intracellular yeast-like symbionts (YLS) in the fat body [3]. YLS occur not only in planthoppers but also in some aphids, scale insects, leafhoppers and cicadas [4][5][6]. The diversity of YLS in rice planthoppers has been recently demonstrated [7][8][9], and has been found to be altered in response to insecticides and environmental factors [10,11].…”

Unity Makes Strength: A Review on Mutualistic Symbiosis in Representative Insect Clades

“…Similarly, there are many cases in which YLS phylogenetically related to the entomopathogenic genus Ophiocordyceps (Ascomycota: Sordariomycetes: Hypocreales) have joined or replaced Sulcia and/or its bacterial partner. Thus, Sulcia has been replaced in some young lineages of Delphacidae planthoppers (Fulgoroidea) [107]; neither Vidania nor Sulcia were found in some young lineages of family Delphacidae where a vertically transmitted YLS was found [107,108]; and the same kind of YLS was found in some leafhoppers of subfamilies Deltocephalinae [109,110,111] and Ledrinae [112], whether replacing Nasuia or in an intermediate stage in which both Nasuia and the YLS coexist with Sulcia . In addition, many independent cases of Hodgkinia replacement have been found in several tribes of two cicadidae subfamilies; in fact, it is possible that repeated Hodgkinia -fungus and fungus–fungus replacements had occurred [85].…”