Elucidation of the transmission patterns of an insect-borne bacterium

Abstract

Quantitative data on modes of transmission are a crucial element in understanding the ecology of microorganisms associated with animals. We investigated the transmission patterns of a gamma-proteobacterium informally known as pea aphid Bemisia-like symbiont (PABS), also known as T-type, which is widely but not universally distributed in natural populations of the pea aphid, Acyrthosiphon pisum. The vertical transmission of PABS to asexual and sexual morphs and sexually produced eggs was demonstrated by a diagnostic PCR-based assay, and the maximum estimated failure rate was 2%. Aphids naturally lacking PABS acquired PABS bacteria administered via the diet, and the infection persisted by vertical transmission for at least three aphid generations. PABS was also detected in two of five aphid honeydew samples tested and in all five siphuncular fluid samples tested but in none of 15 samples of salivary secretions from PABS-positive aphids. However, PABS-negative aphids did not acquire PABS when they were cocultured with PABS-positive aphids; the maximal estimated level of horizontal transmission was 18%. A deterministic model indicated that the force of infection by a horizontal transmission rate of 3% is sufficient to maintain a previously described estimate of the prevalence of PABS-positive aphids (37%), if the vertical transmission rate is 98%. We concluded that PABS infections in A. pisum can be maintained by high vertical transmission rates and occasional horizontal transmission, possibly via the oral route, in the absence of selection either for or against aphids bearing this bacterium.

FIG. 1.

Incidence of horizontal transmission of PABS. (a) Release of PABS from A. pisum line LMB95/28 via siphuncular fluid (lanes 1 to 5), honeydew (lanes 6 to 10), and feeding on diet sachets (lanes 11 to 15). Lane 16 contained a PABS-positive control, and lane 17 contained a negative control. (b) Acquisition of PABS by A. pisum line JF98/24 (lanes 1 and 2) and A. fabae line HR91/3 (lanes 3 and 4) from diet sachets that either bore PABS (lanes 1 and 3) or were microbiologically sterile (lanes 2 and 4). After feeding on the test diets, aphids were reared on plants for three generations prior to analysis. Lane 5 contained a PABS-positive control, and lane 6 contained a negative control. (c) PABS status of A. pisum lines ACD01/04 and LMB95/28 in coculture. ACD01/04 (lane 1) and LMB95/28 (lane 2) were examined at the start of the experiment; one of five replicate aphids of line ACD01/04 from each cage (lanes 3 to 5) and of LMB95/28 from one cage (lane 6) were examined at the end of the experiment. Lane 7 contained a PABS-positive control, and lane 8 contained a negative control.

FIG. 2.

Force of infection in a frequency-dependent model required to maintain the proportion of PABS-positive aphids in a population with 2 to 50% loss through failure of vertical transmission.