Horizontal Transfer of Bacterial Symbionts: Heritability and Fitness Effects in a Novel Aphid Host

Abstract

Members of several bacterial lineages are known only as symbionts of insects and move among hosts through maternal transmission. Such vertical transfer promotes strong fidelity within these associations, favoring the evolution of microbially mediated effects that improve host fitness. However, phylogenetic evidence indicates occasional horizontal transfer among different insect species, suggesting that some microbial symbionts retain a generalized ability to infect multiple hosts. Here we examine the abilities of three vertically transmitted bacteria from the Gammaproteobacteria to infect and spread within a novel host species, the pea aphid, Acyrthosiphon pisum. Using microinjection, we transferred symbionts from three species of natural aphid hosts into a common host background, comparing transmission efficiencies between novel symbionts and those naturally infecting A. pisum. We also examined the fitness effects of two novel symbionts to determine whether they should persist under natural selection acting at the host level. Our results reveal that these heritable bacteria vary in their capacities to utilize A. pisum as a host. One of three novel symbionts failed to undergo efficient maternal transmission in A. pisum, and one of the two efficiently transmitted bacteria depressed aphid growth rates. Although these findings reveal that negative fitness effects and low transmission efficiency can prevent the establishment of a new infection following horizontal transmission, they also indicate that some symbionts can overcome these obstacles, accounting for their widespread distributions across aphids and related insects.

Sexual acquisition of beneficial symbionts in aphids

“…Horizontal transmission within and among species is also demonstrated by molecular phylogenetic analyses (3,16,17). Furthermore, transfections by microinjection of hemolymph from an infected aphid into one with no secondary symbiont or with a different symbiont species or strain yield high rates of establishment as stable heritable symbioses (8,13,18), indicating that these secondary symbionts have the capacity to invade cells, hemocoels, and embryos of naïve hosts. Aphids can also acquire infections from feeding on an artificial diet into which symbionts from infected aphids have been introduced (19).…”

“…In some cases, it was performed on generation 2 or 3. In cases in which quantitative PCR indicated that a paternal symbiont had been acquired, largerscale PCR was performed with a symbiont-specific 16S rRNA primer (R1279F 5Ј-CGAGAGCA AGCGGACCTCAC-3Ј, T1279F 5Ј-CGAGGGAAAGCGGAACTCAG-3Ј, or U1279F 5Ј-CGAACGTAAGCGAACCTCAT-3Ј) combined in each case with a more universal 23S rRNA primer, 35R (18). Amplified 16S rRNA products were sequenced at the Genomic Analysis and Technology Core (GATC) facility (University of Arizona, Tucson, AZ).…”

“…For each cross, 10-15 females in the final juvenile (fourth) instar were placed on an aphid-free plant and caged, and 3-6 males from the chosen line were introduced to the cage. Cages were made from polystyrene cups (18). Females cannot mate before reaching adulthood, so this procedure ensures that females were virgins (i.e., had not mated within their natal colony).…”

Parasitoids as vectors of facultative bacterial endosymbionts in aphids

“…We tested the offspring rather than the recipients themselves because our prime interest was in transmissions resulting in new, heritable infections. The last born offspring were tested because new infections require several days of 'incubation' before they are transmitted maternally [13]. The DNA of individual aphids was prepared with Chelex to test for the presence of either H. defensa or R. insecticola using diagnostic PCR of part of the 16S rRNA gene.…”

Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes

“…The small components are species that are connected by recent LGT events among themselves, but no dLGT was identified between them and species included in the main connected component, on the basis of the present sample. These small groups typically comprise intracellular pathogens or endosymbionts, such as Legionella pneumophila, Leptospira interrogans, and the like, whose host-associated life style is a barrier to LGT, although they are sometimes able to exchange genes among themselves (Russell and Moran 2005). The endosymbiont-specific connected components are an important internal positive control for this directed network approach to LGT, because from the underlying biology of these organisms we know that they should be rarely connected via recent LGT to other species.…”