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

2019 ◽  
Author(s):  
Melanie R. Smee ◽  
Imperio Real-Ramirez ◽  
Tory A. Hendry
Keyword(s):  
Pseudomonas Syringae ◽  
Acyrthosiphon Pisum ◽  
Waste Product ◽  
Insect Herbivores ◽  
Epiphytic Bacteria ◽  
Alternative Host ◽  
Associated Bacteria ◽  
Pea Aphids ◽  
Fitness Benefits ◽  
Diverse Plant

AbstractInsect 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.

scholarly journals Epiphytic strains of Pseudomonas syringae kill diverse aphid species.

2021 ◽  
Author(s):  
Melanie R. Smee ◽  
Imperio Real-Ramirez ◽  
Catalina Zuluaga Arias ◽  
Tory A. Hendry
Keyword(s):  
Biological Control ◽  
Pseudomonas Syringae ◽  
Plant Pathogens ◽  
Acyrthosiphon Pisum ◽  
Rhopalosiphum Padi ◽  
Aphid Species ◽  
Pea Aphid ◽  
Oral Exposure ◽  
Pest Species ◽  
Epiphytic Bacteria

Interactions between epiphytic bacteria and herbivorous insects are ubiquitous on plants, but little is known about their ecological implications. Aphids are devastating crop pests worldwide, and so understanding how epiphytic bacteria impact aphid populations is critically important. Recent evidence demonstrates that plant-associated bacteria, such as Pseudomonas syringae, can be highly virulent to one species of aphid, the pea aphid (Acyrthosiphon pisum). Yet currently we have no knowledge on how broad this phenomenon is across diverse aphid species that are of high agricultural concern. In controlled experiments using oral exposure in artificial diet, we challenged five aphid species of agricultural importance with three strains of P. syringae that vary in virulence to the pea aphid. These strains also vary in epiphytic ability and comprise two phytopathogens and one non-plant pathogenic strain. In general, differences in virulence to aphids remained relatively constant across strains regardless of the aphid species, except for the bird cherry-oat aphid (Rhopalosiphum padi) which is significantly less susceptible to two P. syringae strains. We demonstrate that lower infection incidence likely plays a role in the reduced susceptibility. Importantly, these data support previous results showing that interactions with epiphytic bacteria are important for aphids and may play a large, but underappreciated, role in insect population dynamics. Our study illustrates a potential role of epiphytic bacteria in the biological control of aphid pests broadly, but suggests the need for more research encompassing a greater diversity of pest species. Importance Sap-sucking aphids are insects of huge agricultural concern, not only because of direct damage caused by feeding, but also because of their ability to transmit various plant pathogens. Some bacteria that grow on leaf surfaces, such as Pseudomonas syringae, can infect and kill aphids, making them potentially useful in biological control of pest aphids. However, only one aphid species, the pea aphid (Acyrthosiphon pisum) has been tested for infection by P. syringae. Here we challenged five aphid species of agricultural importance with three strains of P. syringae that vary in virulence to the pea aphid. We found that four of these aphid species were susceptible to infection and death, suggesting that these bacteria could be broadly useful for biological control. However, one aphid species was much more resistant to infection, indicating that more testing on diverse aphid species is needed.

scholarly journals Pea Aphid as both Host and Vector for the Phytopathogenic Bacterium Pseudomonas syringae

2009 ◽  
Vol 75 (7) ◽  
pp. 2230-2235 ◽  
Author(s):  
John Stavrinides ◽  
Jodi K. McCloskey ◽  
Howard Ochman
Keyword(s):  
Pseudomonas Syringae ◽  
Pea Aphid ◽  
Epiphytic Bacteria ◽  
Agricultural Pests ◽  
Bacterial Sepsis ◽  
Phytopathogenic Bacterium ◽  
Mutagenesis Screen ◽  
Pea Aphids ◽  
Bacterial Transmission ◽  
Aphid Honeydew

ABSTRACT Aphids are widespread agricultural pests that are capable of disseminating plant viral diseases; however, despite coming into frequent contact with epiphytic bacteria, aphids are considered to have no role in bacterial transmission. Here, we demonstrate the ability of pea aphids to vector the phytopathogen Pseudomonas syringae pv. syringae B728a (PsyB728a). While feeding on plants colonized by epiphytic bacteria, aphids acquire the bacteria, which colonize the digestive tract, multiply, and are excreted in the aphid honeydew, resulting in inoculation of the phyllosphere with up to 107 phytopathogenic bacteria per cm2. Within days of ingesting bacteria, aphids succumb to bacterial sepsis, indicating that aphids serve as an alternative, nonplant host for PsyB728a. The related strain Pseudomonas syringae pv. tomato DC3000 is >1,000-fold less virulent than PsyB728a in the pea aphid, suggesting that PsyB728a possesses strain-specific pathogenicity factors that allow it to exploit aphids as hosts. To identify these factors, we performed a mutagenesis screen and recovered PsyB728a mutants that were hypovirulent, including one defective in a gene required for flagellum formation and motility. These interactions illustrate that aphids can also vector bacterial pathogens and that even seemingly host-restricted pathogens can have alternative host specificities and lifestyles.

scholarly journals A highly infective plant-associated bacterium influences reproductive rates in pea aphids

2016 ◽  
Vol 3 (2) ◽  
pp. 150478 ◽  
Author(s):  
Tory A. Hendry ◽  
Kelley J. Clark ◽  
David A. Baltrus
Keyword(s):  
Pseudomonas Syringae ◽  
Acyrthosiphon Pisum ◽  
Dependent Manner ◽  
Bacterial Cells ◽  
Pea Aphids ◽  
Survival And Reproduction ◽  
Fecundity Compensation ◽  
Reproductive Rates ◽  
High Doses ◽  
Aphid Pathogen

Pea aphids, Acyrthosiphon pisum , have the potential to increase reproduction as a defence against pathogens, though how frequently this occurs or how infection with live pathogens influences this response is not well understood. Here we determine the minimum infective dose of an environmentally common bacterium and possible aphid pathogen, Pseudomonas syringae , to determine the likelihood of pathogenic effects to pea aphids. Additionally, we used P. syringae infection to investigate how live pathogens may alter reproductive rates. We found that oral bacterial exposure decreased subsequent survival of aphids in a dose-dependent manner and we estimate that ingestion of less than 10 bacterial cells is sufficient to increase aphid mortality. Pathogen dose was positively related to aphid reproduction. Aphids exposed to low bacterial doses showed decreased, although statistically indistinguishable, fecundity compared to controls. Aphids exposed to high doses reproduced significantly more than low dose treatments and also more, but not significantly so, than controls. These results are consistent with previous studies suggesting that pea aphids may use fecundity compensation as a response to pathogens. Consequently, even low levels of exposure to a common plant-associated bacterium may therefore have significant effects on pea aphid survival and reproduction.

scholarly journals Drop when the stakes are high: adaptive, flexible use of dropping behaviour by aphids

Behaviour ◽  
2021 ◽  
pp. 1-21
Author(s):  
Rosalind K. Humphreys ◽  
Graeme D. Ruxton ◽  
Alison J. Karley
Keyword(s):  
Host Plant ◽  
Acyrthosiphon Pisum ◽  
Adalia Bipunctata ◽  
Macrosiphum Euphorbiae ◽  
Herbivorous Insects ◽  
Chrysoperla Carnea ◽  
Pea Aphids ◽  
Potato Aphids ◽  
Antipredator Defence

Abstract For herbivorous insects, dropping from the host plant is a commonly-observed antipredator defence. The use of dropping compared to other behaviours and its timing in relation to contact with a predator was explored in both pea aphids (Acyrthosiphon pisum) and potato aphids (Macrosiphum euphorbiae). Pea aphids dropped more frequently in response to ladybird adults (Adalia bipunctata) than lacewing larvae (Chrysoperla carnea). Potato aphids mainly walked away or backed-up in response to both predator types; but they dropped more frequently relative to other non-walking defences when faced with ladybird adults. Contact with a predator was an important influencer of dropping for both species, and most drops occurred from adjacent to the predator. Dropping appears to be a defence adaptively deployed only when the risk of imminent predation is high; factors that increase dropping likelihood include presence of faster-foraging predators such as adult ladybirds, predator proximity, and contact between aphid and predator.

scholarly journals Location and Survival of Leaf-Associated Bacteria in Relation to Pathogenicity and Potential for Growth within the Leaf

1999 ◽  
Vol 65 (4) ◽  
pp. 1435-1443 ◽  
Author(s):  
M. Wilson ◽  
S. S. Hirano ◽  
S. E. Lindow
Keyword(s):  
Pseudomonas Syringae ◽  
Plant Pathogens ◽  
Vacuum Infiltration ◽  
Associated Bacteria ◽  
Growth And Survival ◽  
Total Leaf ◽  
Spray Inoculation ◽  
Dry Conditions ◽  
Population Sizes ◽  
Better Than

ABSTRACT The growth and survival of pathogenic and nonpathogenicPseudomonas syringae strains and of the nonpathogenic species Pantoea agglomerans, Stenotrophomonas maltophilia, and Methylobacterium organophilum were compared in the phyllosphere of bean. In general, the plant pathogens survived better than the nonpathogens on leaves under environmental stress. The sizes of the total leaf-associated populations of the pathogenic P. syringae strains were greater than the sizes of the total leaf-associated populations of the nonpathogens under dry conditions but not under moist conditions. In these studies the surface sterilants hydrogen peroxide and UV irradiation were used to differentiate cells that were fully exposed on the surface from nonexposed cells that were in “protected sites” that were inaccessible to these agents. In general, the population sizes in protected sites increased with time after inoculation of plants. The proportion of bacteria on leaves that were in protected sites was generally greater for pathogens than for nonpathogens and was greater under dry conditions than under moist conditions. When organisms were vacuum infiltrated into leaves, the sizes of the nonexposed “internal” populations were greater for pathogenic P. syringae strains than for nonpathogenic P. syringaestrains. The sizes of the populations of the nonpathogenic species failed to increase or even decreased. The sizes of nonexposed populations following spray inoculation were correlated with the sizes of nonexposed, internal populations which developed after vacuum infiltration and incubation. While the sizes of the populations of the pathogenic P. syringae strains increased on leaves under dry conditions, the sizes of the populations of the nonpathogenic strains of P. syringae, P. agglomerans, andS. maltophilia decreased when the organisms were applied to plants. The sizes of the populations on dry leaves were also correlated with the sizes of the nonexposed populations that developed following vacuum infiltration. Although pathogenicity was not required for growth in the phyllosphere under high-relative-humidity conditions, pathogenicity apparently was involved in the ability to access and/or multiply in certain protected sites in the phyllosphere and in growth on dry leaves.

SEASONAL ABUNDANCE OF THE PEA APHID, ACYRTHOSIPHON PISUM (HOMOPTERA: APHIDIDAE), IN MANITOBA FIELD PEAS

1986 ◽  
Vol 118 (6) ◽  
pp. 601-607 ◽  
Author(s):  
G.A. Maiteki ◽  
R.J. Lamb ◽  
S.T. Ali-Khan
Keyword(s):  
Pisum Sativum ◽  
Acyrthosiphon Pisum ◽  
Pea Aphid ◽  
Seasonal Abundance ◽  
Economic Threshold ◽  
Field Peas ◽  
Pea Aphids

AbstractPea aphids, Acyrthosiphon pisum (Harris), were sampled from 1980 to 1983 in field peas, Pisum sativum (L.), in Manitoba. Sweep and foliage samples were taken in commercial fields and plots. Aphids were found in late May or early June soon after the crop emerged, but populations were low throughout June. Populations increased in July, when the crop was flowering and producing pods, and peaked in the latter half of July or early August in 3 of the 4 years, when pods were maturing. Populations decreased rapidly after the peak, as the plants senesced. In 1980, a drought year, aphid densities were low and the populations peaked in the middle of August. From 1981 to 1983, densities exceeded the economic threshold in all commercial fields and all but one of the plots that were sampled.

scholarly journals Comparison of ATPase-Encoding Type III Secretion System hrcN Genes in Biocontrol Fluorescent Pseudomonads and in Phytopathogenic Proteobacteria

2004 ◽  
Vol 70 (9) ◽  
pp. 5119-5131 ◽  
Author(s):  
Fabio Rezzonico ◽  
Geneviève Défago ◽  
Yvan Moënne-Loccoz
Keyword(s):  
Pseudomonas Syringae ◽  
Protein Secretion ◽  
Type Iii Secretion ◽  
Fluorescent Pseudomonads ◽  
Secretion Systems ◽  
Associated Bacteria ◽  
Type Iii ◽  
Encoding Gene ◽  
Type Iii Protein Secretion ◽  
Protein Secretion Systems

ABSTRACT Type III protein secretion systems play a key role in the virulence of many pathogenic proteobacteria, but they also occur in nonpathogenic, plant-associated bacteria. Certain type III protein secretion genes (e.g., hrcC) have been found in Pseudomonas sp. strain SBW25 (and other biocontrol pseudomonads), but other type III protein secretion genes, such as the ATPase-encoding gene hrcN, have not been found. Using both colony hybridization and a PCR approach, we show here that hrcN is nevertheless present in many biocontrol fluorescent pseudomonads. The phylogeny of biocontrol Pseudomonas strains based on partial hrcN sequences was largely congruent with the phylogenies derived from analyses of rrs (encoding 16S rRNA) and, to a lesser extent, biocontrol genes, such as phlD (for 2,4-diacetylphloroglucinol production) and hcnBC (for HCN production). Most biocontrol pseudomonads clustered separately from phytopathogenic proteobacteria, including pathogenic pseudomonads, in the hrcN tree. The exception was strain KD, which clustered with phytopathogenic pseudomonads, such as Pseudomonas syringae, suggesting that hrcN was acquired from the latter species. Indeed, strain KD (unlike strain SBW25) displayed the same organization of the hrpJ operon, which contains hrcN, as P. syringae. These results indicate that the occurrence of hrcN in most biocontrol pseudomonads is not the result of recent horizontal gene transfer from phytopathogenic bacteria, although such transfer might have occurred for a minority of biocontrol strains.

INFLUENCE OF STARVATION ON DEVELOPMENT AND REPRODUCTION IN APTEROUS VIRGINOPARAE OF THE PEA APHID, ACYRTHOSIPHON PISUM (HARRIS) (HOMOPTERA: APHIDIDAE)

1992 ◽  
Vol 124 (1) ◽  
pp. 87-95 ◽  
Author(s):  
K.L. Kouamé ◽  
M. Mackauer
Keyword(s):  
Vicia Faba ◽  
Acyrthosiphon Pisum ◽  
Reproductive Investment ◽  
Dry Weight ◽  
Pea Aphid ◽  
Nutrient Loss ◽  
Adult Weight ◽  
Pea Aphids ◽  
Wet Weight ◽  
Growth Development

AbstractThe influence of nutrient stress on growth, development, and reproduction in apterous virginoparae of the pea aphid, Acyrthosiphon pisum (Harris), was investigated in the laboratory. We tested the hypothesis that species with a high reproductive investment have low resistance to starvation. Aphids in two groups were starved daily from birth for 4 h and 6 h, respectively, and compared with feeding counterparts reared on leaves of broad beans, Vicia faba L. Aphid wet weight increased as an exponential function of age in all groups. Starved aphids had lower adult weight and required longer from birth to parturition than feeding aphids. These effects increased with the length of daily starvation. The number of offspring produced was correlated with adult dry weight. Aphids were unable to compensate, or to compensate completely, for water and nutrient loss resulting from starvation. It is suggested that pea aphids allocate resources first to maintenance and then to reproduction when deprived of food.

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