Context-Dependent Benefits of Aphids for Bacteria in the Phyllosphere

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.

Common fluorescent Pseudomonas in the phyllosphere can influence aphid behavior in diverse ways

“…Pellets were washed twice via resuspension with 10mL buffer before adjusting the bacterial suspension to an OD 600 of 1.0 (+/- 0.02). Bacterial suspensions were sprayed onto two-week-old fava bean plants using a sterilized spray bottle (Smee and Hendry 2022). Plants were sprayed until visibly wet but not dripping (about 3 sprays per spray area) and left to dry for one hour in a biosafety cabinet.…”

“…Pellets were washed twice via resuspension with 10mL buffer before adjusting the bacterial suspension to an OD600 of 1.0 (+/-0.02). Bacterial suspensions were sprayed onto twoweek-old fava bean plants using a sterilized spray bottle (Smee and Hendry 2022).…”

“…Bacteria in the genus Pseudomonas (pseudomonads) are common members of phyllosphere communities and are often studied for their direct impacts on plants as pathogens or beneficial taxa (Passera et al 2019; Abdellatif et al 2022; Agbavor et al 2022). However, interactions of pseudomonads with herbivorous insects can also have important ecological outcomes (Humphrey et al 2014; Smee and Hendry 2022). For instance, plant-associated Pseudomonas can influence both the survival and behavior of aphid pest insects (Stavrinides et al 2009; Hendry et al 2016; Smee et al 2021; Smee and Hendry 2022; Silva-Sanzana et al 2023).…”

“…However, interactions of pseudomonads with herbivorous insects can also have important ecological outcomes (Humphrey et al 2014; Smee and Hendry 2022). For instance, plant-associated Pseudomonas can influence both the survival and behavior of aphid pest insects (Stavrinides et al 2009; Hendry et al 2016; Smee et al 2021; Smee and Hendry 2022; Silva-Sanzana et al 2023). Aphids avoid feeding on leaves with epiphytic populations of certain Pseudomonas syringae strains due to fluorescent emissions from bacterially produced compounds (Hendry et al 2018).…”

Exchange of Microbiomes in Plant-Insect Herbivore Interactions

“…A similar observation was made when the effect of pea aphid ( Acyrthosiphon pisum Harris) was studied on the distribution of P. syringae among epiphytic communities, as the bacterium thrived better on aphid-infested leaves. The aphid feeding, attributed to the presence of honeydew, had a pronounced effect on P. syringae populations, which were initially small on the leaves ( 104 ). In beech and oak, the feeding of lepidopterous larvae caused changes in the bacterial communities of the leaves, which were associated with the increase of available nitrogen ( 105 ).…”