Sulcia symbiont of the leafhopper Macrosteles laevis (Ribaut, 1927) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae) harbors Arsenophonus bacteria

Abstract

The leafhopper Macrosteles laevis, like other plant sap-feeding hemipterans, lives in obligate symbiotic association with microorganisms. The symbionts are harbored in the cytoplasm of large cells termed bacteriocytes, which are integrated into huge organs termed bacteriomes. Morphological and molecular investigations have revealed that in the bacteriomes of M. laevis, two types of bacteriocytes are present which are as follows: bacteriocytes with bacterium Sulcia and bacteriocytes with Nasuia symbiont. We observed that in bacteriocytes with Sulcia, some cells of this bacterium contain numerous cells of the bacterium Arsenophonus. All types of symbionts are transmitted transovarially between generations. In the mature female, the bacteria Nasuia, bacteria Sulcia, and Sulcia with Arsenophonus inside are released from the bacteriocytes and start to assemble around the terminal oocytes. Next, the bacteria enter the cytoplasm of follicular cells surrounding the posterior pole of the oocyte. After passing through the follicular cells, the symbionts enter the space between the oocyte and follicular epithelium, forming a characteristic “symbiont ball.”

Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): molecular characterization, ultrastructure and transovarial transmission

“…Previous studies of symbiotic systems in Deltocephalinae leafhoppers have shown that members of this subfamily are characterized by diverse types of symbionts (BUCHNER 1925, 1965, MÜLLER 1962, SACCHI et al 2008, WANGKEEREE et al 2011, NODA et al 2012, ISHII et al 2013, KOBIAŁKA et al 2015. As a rule, the Deltocephalinae leafhoppers harbour the bacterium Sulcia and the betaproteobacterium Nasuia (WANGKEEREE et al 2011, NODA et al 2012, ISHII et al 2013, KOBIAŁKA et al 2015, this study) which MÜLLER (1962) termed a-symbionts and t-symbionts, respectively.…”

“…Recent analyses have shown that in some cicadomorphans (e.g. Aphrophora quadrinotata SAY, 1830, Macrosteles laevis (RIBAUT, 1927)) more than two obligate symbionts may occur (KOGA et al 2013, KOBIAŁKA et al 2015. According to KOGA et al (2013), the presence of three symbionts (i.e.…”

“…As a rule, the Deltocephalinae leafhoppers harbour the bacterium Sulcia and the betaproteobacterium Nasuia (WANGKEEREE et al 2011, NODA et al 2012, ISHII et al 2013, KOBIAŁKA et al 2015, this study) which MÜLLER (1962) termed a-symbionts and t-symbionts, respectively. However, yeast symbionts are present in Scaphoideus titanus (tribe Scaphoideini) , SACCHI et al 2008 and Graphocraerus ventralis (FALLÉN, 1806) (tribe Athysanini) (KOBIAŁKA, in preparation).…”

“…Since recent studies have shown that the Deltocephalinae leafhoppers (SACCHI et al 2008, ISHII et al 2013, KOBIAŁKA et al 2015 contain diverse symbionts, the aim of this study was to characterize the symbiotic system of the common leafhopper D. pulicaris, i.e. the types of symbionts, their ultrastructure, distribution in the body cavity and mode of transovarial transmission.…”

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

“…After the loss of critical translation-related genes in Tremblaya, the symbiosis would persist with a bacteria within a bacterium structure because no other structure is possible. We note that Sodalis-and Arsenophonus-allied symbionts were recently suggested to sometimes reside within Sulcia cells in the leafhoppers Cicadella viridis and Macrosteles laevis (66,67). Although these studies were based only on EM imaging and not confirmed by specific probes (e.g., with FISH), it is possible that symbioses formed by bacteria taking up residence inside of degenerate symbionts with host-derived cell envelopes are not uncommon.…”