Cospeciation of Psyllids and Their Primary Prokaryotic Endosymbionts

Abstract

Psyllids are plant sap-feeding insects that harbor prokaryotic endosymbionts in specialized cells within the body cavity. Four-kilobase DNA fragments containing 16S and 23S ribosomal DNA (rDNA) were amplified from the primary (P) endosymbiont of 32 species of psyllids representing three psyllid families and eight subfamilies. In addition, 0.54-kb fragments of the psyllid nuclear gene wingless were also amplified from 26 species. Phylogenetic trees derived from 16S-23S rDNA and from the host wingless gene are very similar, and tests of compatibility of the data sets show no significant conflict between host and endosymbiont phylogenies. This result is consistent with a single infection of a shared psyllid ancestor and subsequent cospeciation of the host and the endosymbiont. In addition, the phylogenies based on DNA sequences generally agreed with psyllid taxonomy based on morphology. The 3 end of the 16S rDNA of the P endosymbionts differs from that of other members of the domain Bacteria in the lack of a sequence complementary to the mRNA ribosome binding site. The rate of sequence change in the 16S-23S rDNA of the psyllid P endosymbiont was considerably higher than that of other bacteria, including other fast-evolving insect endosymbionts. The lineage consisting of the P endosymbionts of psyllids was given the designation Candidatus Carsonella (gen. nov.) with a single species, Candidatus Carsonella ruddii (sp. nov.).Insects within the families Aphididae (aphids), Psyllidae (psyllids), Aleyrodidae (whiteflies), and Pseudococcidae (mealybugs) feed predominantly or exclusively on plant phloem sap. These insects have a number of common structural properties (8) and constitute separate lineages within the suborder Sternorrhyncha (15, 54). The utilization of plant sap necessitates the penetration of tissue by flexible mouth parts (stylets) and the ingestion of the fluid. This mode of feeding is conducive to the transmission of viruses and other infectious agents, and members of these families are vectors of pathogens of agriculturally important plants (7,28,51). In addition, these insects may reach enormous populations, causing plant nutrient deprivation, leaf curling, and gall formation (8). Plant phloem sap, the diet of these insects, is rich in carbohydrates but deficient in nitrogenous compounds (21,46). Due to this deficiency, a large amount of plant sap is consumed and is excreted as honeydew. This sticky material may cover the plant and serve as a substrate for fungal growth (8).A common feature of organisms that live on diets containing an excess of one class of compounds and a deficiency in essential nutrients is the presence of prokaryotic intracellular symbionts (endosymbionts) that may provide the missing essential nutrients (6, 21, 37). Early histological studies indicated that these endosymbionts are housed within specialized cells (bacteriocytes) that form an aggregate (bacteriome) found within the body cavity (5, 10, 37). Typically, insects of a particular family or superfamily were found to have a ...

Degenerative Minimalism in the Genome of a Psyllid Endosymbiont

“…They are located within host cells called bacteriocytes, where they are enclosed by host-derived membrane vesicles; the multicellular structure containing the bacteriocytes is called a bacteriome (6,7,11,31). In a recent study of 32 psyllid species, the phylogenetic tree derived from the 16S-23S rDNA of C. ruddii agreed with the tree derived from a host gene, a result consistent with a single infection of a psyllid ancestor and subsequent vertical transmission (cospeciation) of endosymbionts and hosts (28). Some psyllid species also contain morphologically diverse secondary (S) endosymbionts (6,11,26); molecular phylogenetic analyses indicate that S-endosymbionts result from multiple infections of hosts and possible horizontal transmission among them (29).…”

“…Phloem sap of most plants is deficient in essential amino acids (23), suggesting that B. aphidicola and the endosymbionts of psyllids have the same functions related to host nutrition. The primary endosymbionts of psyllids, designated Carsonella ruddii, constitute a unique lineage within the ␥ 3 subdivision of the Proteobacteria (11,26,28). They are located within host cells called bacteriocytes, where they are enclosed by host-derived membrane vesicles; the multicellular structure containing the bacteriocytes is called a bacteriome (6,7,11,31).…”

Reductive genome evolution, host–symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies

“…Host-symbiont co-evolution in nycteribiid bat flies Among diverse insect endosymbionts of obligate nature, such as Buchnera of aphids (Moran et al, 1993), Wigglesworthia of tsetse flies (Chen et al, 1999), Carsonella of psyllids (Thao et al, 2000), Portiera of whiteflies (Thao and Baumann, 2004), Sulcia of many homopterans (Moran et al, 2005), Baumannia of sharpshooters (Takiya et al, 2006), Blochmannia of carpenter ants (Sauer et al, 2000), Nardonella of weevils (Conord et al, 2008) and others, the endosymbiont phylogeny generally mirrors the host phylogeny, indicating stable and intimate host-symbiont association over evolutionary time. Our results unequivocally indicate that the endosymbiont of nycteribiid bat flies has experienced a similar co-evolutionary history ( Figure 6).…”

Endosymbiotic Bacteria in Insects: Their Diversity and Culturability

“…Like the aphid-Buchnera endosymbiosis, highly interdependent host-symbiont associations have been found in other insects, such as Wigglesworthia in tsetse flies (24), Baumannia in sharpshooters (79,108), Carsonella in psyllids (110), Tremblaya in mealybugs (109), Blochmannia in carpenter ants (101), Nardonella in weevils (69), and many others (Table 1; Fig. 1).…”