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

Abstract

Insects in the Auchenorrhyncha (Hemiptera: Suborder) established nutritional symbioses with bacteria approximately 300 million years ago (MYA). The suborder split early during its diversification (~ 250 MYA) into the Fulgoroidea (planthoppers) and Cicadomorpha (leafhoppers and cicadas). The two lineages share some symbionts, including Sulcia and possibly a Betaproteobacteria that collaboratively provide their hosts with 10 essential amino acids (EAA). Some hosts harbour three bacteria, as is common among planthoppers. However, genomic studies are currently restricted to the dual-bacterial symbioses found in Cicadomorpha, leaving the origins and functions of these more complex symbioses unclear. To address these questions, we sequenced the genomes and performed phylogenomic analyses of 'Candidatus Sulcia muelleri' (Bacteroidetes), 'Ca. Vidania fulgoroideae' (Betaproteobacteria) and 'Ca. Purcelliella pentastirinorum' (Gammaproteobacteria) from a planthopper (Cixiidae: Oliarus). In contrast to the Cicadomorpha, nutritional synthesis responsibilities are rearranged between the cixiid symbionts. Although Sulcia has a highly conserved genome across the Auchenorrhyncha, in the cixiids it is greatly reduced and provides only three EAAs. Vidania contributes the remaining seven EAAs. Phylogenomic results suggest that it represents an ancient symbiont lineage paired with Sulcia throughout the Auchenorrhyncha. Finally, Purcelliella was recently acquired from plant-insect associated bacteria (Pantoea-Erwinia) to provide B vitamins and metabolic support to its degenerate partners.

Similarities and spatial variations of bacterial and fungal communities in field rice planthopper (Hemiptera: Delphacidae) populations

“…Species in the Auchenorrhyncha (including the cicadas, leafhoppers and spittlebugs) broadly specialize on using phloem and xylem for food and harbor the primary symbiont Sulcia, which may have allied with the Auchenorrhyncha since the origin of the suborder (Moran et al, 2005). The Hawaiian planthopper Oliarus filicicola also harbors Sulcia as a primary symbiont (Bennett & Mao, 2018). However, Sulcia reads were neither observed in our dataset nor in other high-throughput sequencing analyses (Li et al, 2017;Zhang et al, 2018;Zhang et al, 2019;Zhang et al, 2020), suggesting that Sulcia does not exist in rice planthoppers.…”

Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses

“…Organismal scope or featured taxon Cunha & Giribet (2019) yes Gastropods Laumer et al (2019) yes Animals Lemer et al (2019) yes Bivalves Lozano-Fernandez et al (2019) yes Chelicerates Marlétaz et al (2019) yes Spiralia Philippe et al (2019) yes Bilateria Narayanan Kutty et al (2019) no Calyptratae Uribe et al (2019) no Gastropods Wolfe et al (2019) no Decapod crustaceans Zverkov et al (2019) no Dicyemida and Orthonectida Aouad et al (2018) yes Archaea Laumer et al (2018) yes Placozoa Otero-Bravo et al (2018) yes Pantoea Puttick et al (2018) yes Land plants Schwentner et al (2018) yes Pancrustacea Sousa et al (2018) yes Land plants Bennett & Mao (2018) no Fulgoroidea symbionts Eitel et al (2018) no Placozoa Manzano-Marín et al (2018) no Cinara strobi symbionts Feuda et al (2017) yes Animals Szabó et al (2017) yes Pseudococcidae symbionts Williams et al (2017) yes Archaea Schwentner et al (2017) no Pancrustacea Shin et al (2017) no Curculionoidea Simion et al (2017) no Animals Yoshida et al (2017) no Tardigrades Leliaert et al (2016) yes Viridiplantae Zhang et al (2016) yes Roseobacter CHAB-I-5 lineage He et al (2016) no Rhizaria Song et al (2016) no Holometabola Domman et al (2015) yes Plastids Luo (2015) yes SAR11 Petitjean et al (2015) yes Archaea Borowiec et al (2015) no Animals Derelle et al (2015) no Eukaryotes Wang & Wu (2015) no Mitochondria…”

Mutational pressure drives differential genome conservation in two bacterial endosymbionts of sap feeding insects

“…Pairwise divergence estimates for the two ancestral symbionts in closely related leafhopper species (family Cicadellidae) reveal that Sulcia genomes are highly similar (99.68% nucleotide identity), while BetaSymb genomes are 30-fold more divergent (90.47% nucleotide identity) (Bennett, Abbà, et al 2016). The dramatic differences in Sulcia and BetaSymb rates of molecular evolution have also been documented across more divergent auchenorrhynchan lineages (Bennett and Moran 2013;Mao et al 2017;Bennett and Mao 2018).…”

“…BetaSymb (represented by Nasuia in leafhoppers and other names depending on the insect host; Vidani in planthoppers and Zinderia in spittlebugs) evolves much more rapidly that Sulcia, despite the partner endosymbionts having occupied a nearly identical ecological niche (bacteriocytes in a shared host) for ~300 million years (Bennett, Abbà, et al 2016;Bennett and Mao 2018). In addition, BetaSymb experiences increased evolutionary turnover and has been replaced in at least six auchenorrhynchan lineages (Bennett and Moran 2015).…”

“…Comparisons amongst ancient endosymbionts reveal massive variability in genome stability and extinction rates. Insects in the suborder Auchenorrhyncha maintain two bacterial endosymbionts: "Candidatus Sulcia muelleri" (hereafter Sulcia) and a betaproteobacterium (hereafter BetaSymb), which are both thought to be ancestral to the group (~300 Ma) (Moran et al 2005;Dietrich 2009;Bennett and Moran 2013;Bennett and Mao 2018).…”