Degenerative Minimalism in the Genome of a Psyllid Endosymbiont

Abstract

Psyllids, like aphids, feed on plant phloem sap and are obligately associated with prokaryotic endosymbionts acquired through vertical transmission from an ancestral infection. We have sequenced 37 kb of DNA of the genome of Carsonella ruddii, the endosymbiont of psyllids, and found that it has a number of unusual properties revealing a more extreme case of degeneration than was previously reported from studies of eubacterial genomes, including that of the aphid endosymbiont Buchnera aphidicola. Among the unusual properties are an exceptionally low guanine-plus-cytosine content (19.9%), almost complete absence of intergenic spaces, operon fusion, and lack of the usual promoter sequences upstream of 16S rDNA. These features suggest the synthesis of long mRNAs and translational coupling. The most extreme instances of base compositional bias occur in the genes encoding proteins that have less highly conserved amino acid sequences; the guanine-plus-cytosine content of some protein-coding sequences is as low as 10%. The shift in base composition has a large effect on proteins: in polypeptides of C. ruddii, half of the residues consist of five amino acids with codons low in guanine plus cytosine. Furthermore, the proteins of C. ruddii are reduced in size, with an average of about 9% fewer amino acids than in homologous proteins of related bacteria. These observations suggest that the C. ruddii genome is not subject to constraints that limit the evolution of other known eubacteria.

The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes

“…At about 1.7 Mb, its genome is small relative to those of free-living Enterobacteriaceae, which are typically 4-6 Mb, and it is compositionally biased (39% GϩC). However, neither the size nor base composition is as extreme as those observed in long-term primary symbionts, such as B. aphidicola (22), Wigglesworthia glossinidia (37), Blochmannia (38), or Carsonella ruddii (39). All of these organisms have genome sizes Ͻ1 Mb and genomic base compositions of 18-28% GϩC.…”

Tissue Localization of the Endosymbiotic Bacterium “ Candidatus Blochmannia floridanus” in Adults and Larvae of the Carpenter Ant Camponotus floridanus

“…The long-lasting vertical transmission of the various endosymbionts, estimated in the range of 50 million to 250 million years, resulted in congruent phylogenetic trees of the symbiotic partners, demonstrating a long-lasting cospeciation of the bacteria and their host animals. Such a cospeciation of the bacteria and their host organisms is well documented in several cases including the Buchnera, Wigglesworthia, and "Candidatus Blochmannia" insect symbioses (2,7,8,17,20). However, little is known about the transmission process itself, and conflicting accounts exist in the literature.…”

“…The members of this genus are most closely related to other endosymbiotic bacteria of insects such as Buchnera aphidicola of aphids, Wigglesworthia glossinidia of tsetse flies, and, more distantly, Carsonella ruddii of psyllids (2,7,8,17,20). Buchnera, Wigglesworthia, and "Candidatus Blochmannia" form a huge clade of symbiotic microorganisms related to the family of the Enterobacteriaceae within the ␥ subgroup of Proteobacteria.…”

Endosymbiotic Bacteria in the Esophageal Organ of Glossiphoniid Leeches

“…It has been suggested that small population size and lack of effective recombination in vertically transmitted microorganisms result in the accumulation of mildly deleterious mutations, which could be detected as faster sequence evolution and a shift in base composition that reflects mutational bias (19). In fact, essential primary symbionts of insects such as Buchnera aphidicola in aphids and Carsonella ruddii in psyllids exhibit highly AT-biased genomes (4,24). In this context, the AT-biased nucleotide composition may favor the idea that the glossiphoniid leeches and the symbionts have been in an intimate endosymbiotic association over a long evolutionary time.…”