Insects as phyllosphere microbiome engineers: effects of aphids on a plant pathogen.

Abstract

Insect herbivores are common in the phyllosphere, the above-ground parts of plants, and encounter diverse plant-associated bacteria there, yet how these organisms interact remains largely unknown. Strains of the bacterium Pseudomonas syringae grow well epiphytically and have been shown to grow within and kill hemipteran insects like the pea aphid, Acyrthosiphon pisum. Aphids are hypothesized to be an alternative host for these epiphytic bacteria but it is unclear if aphids provide fitness benefits to these bacterial pathogens. To determine if epiphytic bacteria could be adapted for infecting aphids, we characterized 21 strains of P. syringae for epiphytic ability and virulence to pea aphids and found that the two traits were positively correlated. For a subset of strains, we tested if the bacteria derived a fitness benefit from the presence of aphids. Some strains benefited significantly, with up to 18.9% higher population densities when aphids were present, and lower starting population density was predictive of higher benefit from aphid presence. However, further investigation found that honeydew, the sugary waste product of aphids, and not growth in aphids, increased P. syringae growth on leaves. This suggests that aphids may be important microbiome engineers in the phyllosphere, but evolutionarily dead-ends for epiphytic bacteria.