Localization and morphological variation of three bacteriome‐inhabiting symbionts within a planthopper of the genus Oliarus (Hemiptera: Cixiidae)

Abstract

Many planthoppers of the family Cixiidae (Hemiptera: Fulgoroidea) host three bacteriome-inhabiting bacteria: a gammaproteobacterium: 'Ca.Purcelliella pentastirinorum', a betaproteobacterium: 'Ca. Vidania fulgoroidea', and a member of the bacteroidetes: 'Ca.Sulcia muelleri'. Through light microscopy observations, DGGE PCR and FISH analysis, we examined the morphology and localization of these three endosymbionts within the abdomens of females of the planthopper Oliarus filicicola. Our results indicate a complex distribution and variation in bacterial morphologies. 'Ca. Sulcia muelleri' singularly colonize one pair of bacteriomes and have cells of irregular shape with an average diameter of approximately 4-5 μm. 'Ca.Purcelliella pentastirinorum' bacteria are roughly globular and have an average diameter of approximately 1.5-2 μm in a pair of bacteriomes located near the posterior end of the abdomen, which are surrounded by giant and highly degenerated cells of 'Ca.Vidania fulgoroidea'. In addition, 'Ca.Vidania fulgoroidea' colonizes the 'rectal organ' (sensu Buchner) and the bacterial cells appear as a small, roughly globular with an average diameter of 3 μm; whereas, 'Ca.Purcelliella pentastirinorum' infects an additional two bacteriomes and the bacterial cells appear tightly packed and highly degenerated. All three endosymbionts colocalize in the forming eggs inside the host's ovaries. Based on the abdominal distribution of bacteriomes and bacterial morphologies, we suggest that 'Ca.Vidania fulgoroidea' and 'Ca.Purcelliella pentastirinorum' correspond to the symbionts described by Buchner as the 'x-' and the 'c + d symbiont' respectively.

Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages

“…In the Cixiidae planthoppers, Sulcia and Vidania are joined by a third bacterium, Purcelliella . This symbiont is found throughout multiple host genera and sequestered to its own bacteriome, suggesting a stably fixed symbiosis (Urban and Cryan, ; Bressan and Mulligan, ). The genomes of these symbionts reveal that a complex jigsaw of all three partners achieves a complete nutritional symbiosis.…”

“…To better understand the symbiotic roles and origins of Sulcia , Vidania and Purcelliella , we sequenced their complete genomes from a Hawaiian planthopper, Oliarus filicicola (Cixiidae: OLIH). Previous work verified that these three bacteria are obligately intracellular, with each sequestered to distinct bacteriome organs (Buchner, ; Gonella et al ., ; Bressan et al, ; Bressan and Mulligan, ; Michalik et al ., ). Our results reveal that Sulcia may have allied with Vidania since the origin of the Auchenorrhyncha.…”

“…Examples include a Sodalis-like (SL) symbiont (Gammaproteobacteria) in Aphrophoridae spittlebugs and 'Ca. Purcelliella pentastirinorum' (Gammaproteobacteria) and several others among the planthoppers (Gonella et al, 2011;Urban and Cryan, 2012;Bressan et al, 2009;Bressan and Mulligan, 2013;Koga et al, 2013). In the former example, the SL-symbiont replaced Zinderia in some host species and its genome exhibits signatures of recent genomic streamlining and decay Koga and Moran, 2014).…”

Bacterial diversity of bacteriomes and organs of reproductive, digestive and excretory systems in two cicada species (Hemiptera: Cicadidae)

“…muelleri is an a-symbiont of Auchenorrhyncha [34], which has co-evolved with the lineage for more than 260 million years [6], and has been retained in most descendant lineages but lost in some [35]. This bacterium has been observed in the bacteriomes of different leafhoppers [36,37], planthoppers [38], and cicadas including Diceroprocta semicincta (Davis), Magicicada septendecim (Linnaeus) and Tettigetta mariae (Quartau & Boulard) [5,39]. Genomic analyses on S .…”

Small, Smaller, Smallest: The Origins and Evolution of Ancient Dual Symbioses in a Phloem-Feeding Insect

“…The focal symbionts, Nasuia and Sulcia from Macrosteles quadrilineatus (Cicadellidae: Deltocephalinae), are demarcated with a blue and red arrow, respectively. Phylogenies show evolutionary events in symbioses based on molecular phylogenetic studies (Moran et al 2003, 2005; Takiya et al 2006; Urban and Cryan 2012; Noda et al 2012; Bressan and Mulligan 2013; Hou et al 2013; Koga et al 2013). Events are color-coded as follows: Host insect phylogeny (from Cryan and Urban 2012) gray background; Sulcia , red; betaproteobacterial symbiont lineage ( BetaSymb = Zinderia + Nasuia + Vidania ), blue; symbiont loss, black dashed line; and symbiont replacement, green.…”