Spiroplasma Symbiont of the Pea Aphid, Acyrthosiphon pisum (Insecta: Homoptera)

ABSTRACT From a laboratory strain of the pea aphid, Acyrthosiphon pisum, we discovered a previously unknown facultative endosymbiotic bacterium. Molecular phylogenetic analysis based on 16S ribosomal DNA revealed that the bacterium is a member of the genusSpiroplasma. The Spiroplasma organism showed stable vertical transmission through successive generations of the host. Injection of hemolymph from infected insects into uninfected insects established a stable infection in the recipients. TheSpiroplasma symbiont exhibited negative effects on growth, reproduction, and longevity of the host, particularly in older adults. Of 58 clonal strains of A. pisum established from natural populations in central Japan, 4 strains possessed theSpiroplasma organism.

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Intraspecific variation in symbiont density in an insect-microbe symbiosis

10.1101/2020.11.03.365353 ◽

2020 ◽

Author(s):

Benjamin J. Parker ◽

Jan Hrček ◽

Ailsa H.C. McLean ◽

Jennifer A. Brisson ◽

H. Charles J. Godfray

Keyword(s):

Intraspecific Variation ◽

Fungal Pathogens ◽

Acyrthosiphon Pisum ◽

Natural Populations ◽

Pea Aphid ◽

Optimal Density ◽

Evolutionary Forces ◽

Standing Variation ◽

Dramatic Decline

AbstractMany insects host vertically-transmitted microbes, which can confer benefits to their hosts but are costly to maintain and regulate. A key feature of these symbioses is variation: for example, symbiont density can vary among host and symbiont genotypes. However, the evolutionary forces maintaining this variation remain unclear. We studied variation in symbiont density using the pea aphid (Acyrthosiphon pisum) and the bacterium Regiella insecticola, a symbiont that can protect its host against fungal pathogens. We found that relative symbiont density varies both between two Regiella phylogenetic clades and among aphid ‘biotypes’. Higher-density symbiont infections are correlated with stronger survival costs, but variation in density has little effect on the protection Regiella provides against fungus. Instead, we found that in some aphid genotypes, a dramatic decline in symbiont density precedes the loss of a symbiont infection. Together, our data suggest that the optimal density of a symbiont infection is likely different from the perspective of aphid and microbial fitness. Regiella might prevent loss by maintaining high within-host densities, but hosts do not appear to benefit from higher symbiont numbers and may be advantaged by losing costly symbionts in certain environments. The standing variation in symbiont density observed in natural populations could therefore be maintained by antagonistic coevolutionary interactions between hosts and their symbiotic microbes.

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Faculty Opinions recommendation of Characterization of a facultative endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1023448.285718 ◽

2005 ◽

Author(s):

Robert Goodman

Keyword(s):

Acyrthosiphon Pisum ◽

Pea Aphid ◽

Endosymbiotic Bacterium

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Rickettsia Symbiont in the Pea Aphid Acyrthosiphon pisum: Novel Cellular Tropism, Effect on Host Fitness, and Interaction with the Essential Symbiont Buchnera

Applied and Environmental Microbiology ◽

10.1128/aem.71.7.4069-4075.2005 ◽

2005 ◽

Vol 71 (7) ◽

pp. 4069-4075 ◽

Cited By ~ 170

Author(s):

Makiko Sakurai ◽

Ryuichi Koga ◽

Tsutomu Tsuchida ◽

Xian-Ying Meng ◽

Takema Fukatsu

Keyword(s):

Acyrthosiphon Pisum ◽

Natural Populations ◽

Pea Aphid ◽

Host Cells ◽

Pcr Analysis ◽

Bacterial Cells ◽

Host Fitness ◽

Host Aphid ◽

Sheath Cells

ABSTRACT In natural populations of the pea aphid Acyrthosiphon pisum, a facultative bacterial symbiont of the genus Rickettsia has been detected at considerable infection frequencies worldwide. We investigated the effects of the Rickettsia symbiont on the host aphid and also on the coexisting essential symbiont Buchnera. In situ hybridization revealed that the Rickettsia symbiont was specifically localized in two types of host cells specialized for endosymbiosis: secondary mycetocytes and sheath cells. Electron microscopy identified bacterial rods, about 2 μm long and 0.5 μm thick, in sheath cells of Rickettsia-infected aphids. Virus-like particles were sometimes observed in association with the bacterial cells. By an antibiotic treatment, we generated Rickettsia-infected and Rickettsia-eliminated aphid strains with an identical genetic background. Comparison of these strains revealed that Rickettsia infection negatively affected some components of the host fitness. Quantitative PCR analysis of the bacterial population dynamics identified a remarkable interaction between the coexisting symbionts: Buchnera population was significantly suppressed in the presence of Rickettsia, particularly at the young adult stage, when the aphid most actively reproduces. On the basis of these results, we discussed the possible mechanisms that enable the prevalence of Rickettsia infection in natural host populations in spite of the negative fitness effects observed in the laboratory.

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Characterization of a Facultative Endosymbiotic Bacterium of the Pea Aphid Acyrthosiphon pisum

Microbial Ecology ◽

10.1007/s00248-004-0216-2 ◽

2005 ◽

Vol 49 (1) ◽

pp. 126-133 ◽

Cited By ~ 49

Author(s):

T. Tsuchida ◽

R. Koga ◽

X.Y. Meng ◽

T. Matsumoto ◽

T. Fukatsu

Keyword(s):

Acyrthosiphon Pisum ◽

Pea Aphid ◽

Endosymbiotic Bacterium

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A small set of differentially expressed genes was associated with two color morphs in natural populations of the pea aphid Acyrthosiphon pisum

Gene ◽

10.1016/j.gene.2018.01.079 ◽

2018 ◽

Vol 651 ◽

pp. 23-32 ◽

Cited By ~ 5

Author(s):

Li Zhang ◽

Meng-Yao Wang ◽

Xiao-Peng Li ◽

Xiao-Tong Wang ◽

Cheng-Lin Jia ◽

...

Keyword(s):

Differentially Expressed Genes ◽

Acyrthosiphon Pisum ◽

Natural Populations ◽

Pea Aphid ◽

Differentially Expressed ◽

Color Morphs ◽

Small Set

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Elucidation of the Transmission Patterns of an Insect-Borne Bacterium

Applied and Environmental Microbiology ◽

10.1128/aem.69.8.4403-4407.2003 ◽

2003 ◽

Vol 69 (8) ◽

pp. 4403-4407 ◽

Cited By ~ 70

Author(s):

A. C. Darby ◽

A. E. Douglas

Keyword(s):

Vertical Transmission ◽

Acyrthosiphon Pisum ◽

Deterministic Model ◽

Transmission Rate ◽

Horizontal Transmission ◽

Natural Populations ◽

Oral Route ◽

Pea Aphid ◽

Diagnostic Pcr ◽

Modes Of Transmission

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 γ-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.

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Unravelling the genomic basis and evolution of the pea aphid male wing dimorphism

10.1101/156133 ◽

2017 ◽

Cited By ~ 1

Author(s):

Binshuang Li ◽

Ryan D. Bickel ◽

Benjamin J. Parker ◽

Neetha Nanoth Vellichirammal ◽

Mary Grantham ◽

...

Keyword(s):

Complex Traits ◽

Acyrthosiphon Pisum ◽

Natural Populations ◽

Pea Aphid ◽

Specific Gene ◽

Regulatory Change ◽

Wing Dimorphism ◽

Wing Polymorphism ◽

Male Wing ◽

Mechanistic Basis

SummaryWing dimorphisms have long served as models for examining the ecological and evolutionary tradeoffs associated with alternative morphologies [1], yet the mechanistic basis of morph determination remains largely unknown. Here we investigate the genetic basis of the pea aphid (Acyrthosiphon pisum) wing dimorphism, wherein males exhibit one of two alternative morphologies that differ dramatically in a set of correlated traits that inclused the presence or absence of wings [2-4]. Unlike the environmentally-induced asexual female aphid wing polyphenism [5], the male wing polymorphism is genetically determined by a single uncharacterized locus on the X chromosome called aphicarus (“aphid” plus “Icarus”, api) [6, 7]. Using recombination and association mapping, we localized api to a 130kb region of the pea aphid genome. No nonsynonymous variation in coding sequences strongly associated with the winged and wingless phenotypes, indicating that api is likely a regulatory change. Gene expression level profiling revealed an aphid-specific gene from the region expressed at higher levels in winged male embryos, coinciding with the expected stage of api action. Comparison of the api region across biotypes (pea aphid populations specialized to different host plants that began diverging ~16,000 years ago [8, 9]) revealed that the two alleles were likely present prior to biotype diversification. Moreover, we find evidence for a recent selective sweep of a wingless allele since the biotypes diversified. In sum, this study provides insight into how adaptive, complex traits evolve within and across natural populations.

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