Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi

Abstract

We have identified and completely sequenced a novel plasmid isolated from the aphid Rhopalosiphum padi. Evidence which suggests that the plasmid occurs localized within the bacterial endosymbionts is presented. The plasmid contains the four genes that constitute the entire leucine operon. This fact makes it really unique since most plasmids are dispensable and lack genes that encode essential anabolic functions. Four more phloem-feeding aphid species also seem to contain homologous plasmids. Although further work is necessary, we hypothesize that this plasmid has appeared during the evolution of the symbiotic association between the aphid and the bacterial endosymbiont. The fact that this plasmid contains the entire leucine operon can be related to physiological evidence showing that the aphid host's diet of plant phloem is deficient in essential amino acids.

Vertical Transmission of Biosynthetic Plasmids in Aphid Endosymbionts ( Buchnera )

“…A recent study found congruence of gene genealogies in Buchnera of Uroleucon ambrosiae, suggesting strictly vertical transfer even within the same host species (22). These results support previous conclusions of congruence among Buchnera genealogies and contribute to the larger picture of vertical plasmid transmission across millions of years (5,6,10,48,49,52,63,64). Our data suggest that the single proposed instance of plasmid transfer in Buchnera may represent a very rare event that occurred early in the evolution of the Pemphigidae (62).…”

“…In contrast to facultative symbionts such as Rhizobium and Vibrio, lateral gene transfer in Buchnera may be highly constrained since this obligate symbiont spends its entire life cycle within specialized host cells (bacteriocytes) (11,43). In accordance with this hypothesis, several previous studies show phylogenetic congruence among chromosomal (trpB and 16S rRNA) and plasmid (trpEG and leuABCD) genes of Buchnera associated with the family Aphididae and suggest a lack of plasmid transfer in this symbiont group (5,6,10,22,48,49,51,63,64). However, recent work suggests horizontal transfer of the plasmid-encoded repA1 gene in Buchnera of Pemphigus spyrothecae (62).…”

“…In Buchnera aphidicola, the primary endosymbiont of aphids, genes for the biosynthesis of tryptophan (trpEG) and leucine (leuABCD) often occur on multicopy plasmids (pTrpEG and pLeu, respectively) (5,6,10,31,48,49,52,63,64). Comparative sequence analysis indicates that the ancestral location for both trpEG and leuABCD genes was the Buchnera chromosome, not an exogenous plasmid (7,49,63).…”

Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life

“…During this coevolutionary process, Buchnera suffered considerable genomic changes (i.e., a great reduction in genome size, an increased AϩT bias, great accumulation of deleterious mutations, and the amplification of genes involved in amino acid biosynthesis) (16)(17)(18). Because pathogenic intracellular bacteria with small genomes display a wide variation in chromosome length, it would also be expected that Buchnera of different aphid lineages differ in genome size and gene content.…”

Chromosomal stasis versus plasmid plasticity in aphid endosymbiont Buchnera aphidicola

“…In recent years, genes encoding key enzymes in the pathways leading to tryptophan and leucine biosynthesis (trpEG and leuABCD, respectively) were found to be translocated from the chromosome to plasmids (Lai et al, 1994;Bracho et al, 1995). Amplification of plasmids for essential amino-acid biosynthesis was considered as an indication that B. aphidicola is able to overproduce these nutrients for the benefit of its host and, hence, an adaptation to its symbiotic lifestyle.…”