Structural diversity of symbionts and related cellular mechanisms underlying vertical symbiont transmission in cicadas

Abstract

Summary 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.

Efficient compartmentalization in insect bacteriomes protects symbiotic bacteria from host immune system

“…The compartmentalization strategy sequesters the symbionts in specialized cells, creating a favorable environment for their metabolic activity, and keeping them under control while avoiding overproliferation and virulence. The bacteriomes are therefore found in many insect species, including aphids [55], planthoppers [56], cicadas [57], and beetles [58]. Although very common, little is known about the evolution and immune modulation inside the bacteriomes, as well as on their formation and maintenance.…”

Efficient compartmentalization in insect bacteriomes protects symbiotic bacteria from host immune system

“…The compartmentalization strategy sequesters the symbionts in specialized cells, creating a favorable environment for their metabolic activity and keeping them under control while avoiding overproliferation and virulence. The bacteriomes are therefore found in many insect species, including aphids [ 55 ], planthoppers [ 56 ], cicadas [ 57 ], and beetles [ 58 ]. Although very common, little is known about the evolution and immune modulation inside the bacteriomes, as well as their formation and maintenance.…”

Complex co‐evolutionary relationships between cicadas and their symbionts

“…In the present study, we investigated the co-evolution of cicadas and related symbionts, in particular YLS, based mainly on 28 cicada species from one of our recent studies (Wang et al, 2021a) and 18 cicada species from other previous studies (Van Leuven et al, 2014;Campbell et al, 2015;Matsuura et al, 2018;Łukasik et al, 2019). However, Huechys sanguinea (De Geer) in Wang et al (2021a) was a misidentification, which should be Huechys thoracica Distant based on reidentification of morphology combined with COI barcoding sequence. Herein, we correct this misidentification in Wang et al (2021a).…”

“…However, Huechys sanguinea (De Geer) in Wang et al (2021a) was a misidentification, which should be Huechys thoracica Distant based on reidentification of morphology combined with COI barcoding sequence. Herein, we correct this misidentification in Wang et al (2021a). Further details for DNA extraction and PCR amplification methods, molecular phylogenetic and dating analyses, and diversification of Ophiocordyceps can be found in the Supporting Information.…”

“…Buchner (1965) suggested that fungal symbionts were not as highly adapted when compared to bacterial symbionts, as they tended to be found free in the haemolymph or fat bodies rather than housed in particular host cells. However, previous studies revealed that YLS can be harboured in both the fat bodies and the peripheral bacteriocytes and sheath cells of bacteriomes in a few cicada species (Matsuura et al ., 2018; Wang et al ., 2021a). It has been predicted that YLS in related host insects evolved from parasitizing Ophiocordyceps fungi that have undergone a switch in transmission strategy from horizontal to vertical (Ewald, 1987; Suh et al ., 2001; McCutcheon et al ., 2019).…”