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Structural diversity of symbionts and related cellular mechanisms underlying vertical symbiont transmission in cicadas
Authors:Dandan Wang  Zhi Huang  Johan Billen  Guoyun Zhang  Hong He  Cong Wei
Institution:1. Key Laboratory of Plant Protection Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi, 712100 China

State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi, 712100 China;2. State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi, 712100 China

Key Laboratory of National Forestry and Grassland Administration for Control of Forest Biological Disasters in Western China, College of Forestry, Northwest A&F University, Yangling, Shaanxi, 712100 China;3. Zoological Institute, University of Leuven, Leuven, Naamsestraat 59, B-3000 Belgium;4. State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi, 712100 China;5. Key Laboratory of National Forestry and Grassland Administration for Control of Forest Biological Disasters in Western China, College of Forestry, Northwest A&F University, Yangling, Shaanxi, 712100 China;6. Key Laboratory of Plant Protection Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi, 712100 China

Abstract:Many insects depend on symbiont(s) for survival. This is particularly the case for sap-feeding hemipteran insects. In this study, we revealed that symbionts harboured in cicadas are diverse and complex, and the yeast-like fungal symbionts (YLS) are present in most cicada species, but Hodgkinia is absent. During vertical transmission, Sulcia became swollen with the outer membrane drastically changed, while Hodgkinia became shrunken and changed from irregular to roughly spherical. Sulcia and/or Hodgkinia were exocytosed from the bacteriocytes to the intercellular space of bacteriomes, where they gathered together and were extruded to haemolymph. YLS and associated facultative symbiont(s) in the fat bodies were released to the haemolymph based on bacteriocyte disintegration. The obligate symbiont(s) were endocytosed and exocytosed successively by the epithelial plug cells of the terminal oocyte, while associated facultative symbiont(s), and possibly also YLS, may take a ‘free ride’ on the transmission of obligate symbiont(s) to gain entry into the oocyte. Then, the intermixed symbionts formed a characteristic ‘symbiont ball’ in the oocyte. Our results suggest that YLS in cicadas represent a new example of a relatively early stage of symbiogenesis in insects and contribute to a better understanding of the diversity and transmission mechanisms of symbionts in insects.
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