Worldwide Populations of the Aphid Aphis craccivora Are Infected with Diverse Facultative Bacterial Symbionts

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Many insects are associated with heritable symbionts that mediate ecological interactions, including host protection against natural enemies. The cowpea aphid, Aphis craccivora, is a polyphagous pest that harbors Hamiltonella defensa, which defends against parasitic wasps. Despite this protective benefit, this symbiont occurs only at intermediate frequencies in field populations. To identify factors constraining H. defensa invasion in Ap. craccivora, we estimated symbiont transmission rates, performed fitness assays, and measured infection dynamics in population cages to evaluate effects of infection. Similar to results with the pea aphid, Acyrthosiphon pisum, we found no consistent costs to infection using component fitness assays, but we did identify clear costs to infection in population cages when no enemies were present. Maternal transmission rates of H. defensa in Ap. craccivora were high (ca. 99%) but not perfect. Transmission failures and infection costs likely limit the spread of protective H. defensa in Ap. craccivora. We also characterized several parameters of H. defensa infection potentially relevant to the protective phenotype. We confirmed the presence of H. defensa in aphid hemolymph, where it potentially interacts with endoparasites, and performed real-time quantitative PCR (qPCR) to estimate symbiont and phage abundance during aphid development. We also examined strain variation of H. defensa and its bacteriophage at multiple loci, and despite our lines being collected in different regions of North America, they were infected with a nearly identical strains of H. defensa and APSE4 phage. The limited strain diversity observed for these defensive elements may result in relatively static protection profile for this defensive symbiosis.

Section: Discussionsupporting

confidence: 63%

Section: Discussionmentioning

confidence: 79%

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Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids

Dykstra

Weldon

Martinez

et al. 2014

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“…A phids harbor two types of bacterial endosymbionts: the obligate symbiont Buchnera aphidicola, which occurs in almost all aphids, and facultative bacteria belonging to a variety of taxa that are not essential for aphid survival and typically are found in some but not all individuals of a population (1)(2)(3). The association between Buchnera and aphids was established 80 to 150 million years ago (4), and because transmission is strictly maternal, bacteria and host phylogenies are perfectly congruent.…”

mentioning

confidence: 99%

Host Plant Determines the Population Size of an Obligate Symbiont (Buchnera aphidicola) in Aphids

Zhang

Cao

Zhong

et al. 2016

bBuchnera aphidicola is an obligate endosymbiont that provides aphids with several essential nutrients. Though much is known about aphid-Buchnera interactions, the effect of the host plant on Buchnera population size remains unclear. Here we used quantitative PCR (qPCR) techniques to explore the effects of the host plant on Buchnera densities in the cotton-melon aphid, Aphis gossypii. Buchnera titers were significantly higher in populations that had been reared on cucumber for over 10 years than in populations maintained on cotton for a similar length of time. Aphids collected in the wild from hibiscus and zucchini harbored more Buchnera symbionts than those collected from cucumber and cotton. The effect of aphid genotype on the population size of Buchnera depended on the host plant upon which they fed. When aphids from populations maintained on cucumber or cotton were transferred to novel host plants, host survival and Buchnera population size fluctuated markedly for the first two generations before becoming relatively stable in the third and later generations. Host plant extracts from cucumber, pumpkin, zucchini, and cowpea added to artificial diets led to a significant increase in Buchnera titers in the aphids from the population reared on cotton, while plant extracts from cotton and zucchini led to a decrease in Buchnera titers in the aphids reared on cucumber. Gossypol, a secondary metabolite from cotton, suppressed Buchnera populations in populations from both cotton and cucumber, while cucurbitacin from cucurbit plants led to higher densities. Together, the results suggest that host plants influence Buchnera population processes and that this may provide phenotypic plasticity in host plant use for clonal aphids.A phids harbor two types of bacterial endosymbionts: the obligate symbiont Buchnera aphidicola, which occurs in almost all aphids, and facultative bacteria belonging to a variety of taxa that are not essential for aphid survival and typically are found in some but not all individuals of a population (1-3). The association between Buchnera and aphids was established 80 to 150 million years ago (4), and because transmission is strictly maternal, bacteria and host phylogenies are perfectly congruent. Buchnera is essential for the aphid, and if the symbiont is experimentally removed, the host grows very slowly and cannot reproduce (5-7). Buchnera synthesizes essential amino acids and other substances that are absent in the aphid's phloem diet (1,(8)(9)(10)(11)(12)(13) and is active in purine metabolism (14, 15). The symbiont's activities can be disrupted by heat shock, and it has been shown that variation in the promoter of a Buchnera heat shock gene impacts aphid thermal tolerance (16,17). The genome of Buchnera is much smaller than those of its free-living relatives (18, 19) and in many ways it now resembles an organelle, highly integrated within the physiology of its host.Densities of Buchnera (as measured by quantitative PCR [qPCR] relative to the host) are affected by host age and genotype and by ...

“…It should be noted that, considering the relatively small sample sizes subjected to cloning and sequencing of the bacterial 16S rRNA gene, other facultative symbionts may remain undetected in natural populations of A. thunbergii. The high levels of symbiont coinfections in A. thunbergii (Table 3) are striking but not exceptional: a number of recent studies have revealed frequent coinfections with multiple symbiotic bacteria in natural insect populations (40)(41)(42)(43).…”

Section: Resultsmentioning

confidence: 99%

Bacterial Symbionts of a Devastating Coffee Plant Pest, the Stinkbug Antestiopsis thunbergii (Hemiptera: Pentatomidae)

Matsuura

Hosokawa

Serracin

et al. 2014

dStinkbugs of the genus Antestiopsis, so-called antestia bugs or variegated coffee bugs, are notorious pests of coffee plants in Africa. We investigated the symbiotic bacteria associated with Antestiopsis thunbergii, a major coffee plant pest in Rwanda. PCR, cloning, sequencing, and phylogenetic analysis of bacterial genes identified four distinct bacterial lineages associated with A. thunbergii: a gammaproteobacterial gut symbiont and symbionts representing the genera Sodalis, Spiroplasma, and Rickettsia. In situ hybridization showed that the gut symbiont densely occupied the lumen of midgut crypts, whereas the Sodalis symbiont, the Spiroplasma symbiont, and the Rickettsia symbiont sparsely and sporadically infected various cells and tissues. Diagnostic PCR survey of 154 A. thunbergii individuals collected at 8 localities in Rwanda revealed high infection frequencies (100% for the gut symbiont, 51.3% for the Sodalis symbiont, 52.6% for the Spiroplasma symbiont, and 24.0% for the Rickettsia symbiont). These results suggest that the gut symbiont is the primary symbiotic associate of obligate nature for A. thunbergii, whereas the Sodalis symbiont, the Spiroplasma symbiont, and the Rickettsia symbiont are the secondary symbiotic associates of facultative nature. We observed high coinfection frequencies, i.e., 7.8% of individuals with quadruple infection with all the symbionts, 32.5% with triple infections with the gut symbiont and two of the secondary symbionts, and 39.6% with double infections with the gut symbiont and any of the three secondary symbionts, which were statistically not different from the expected coinfection frequencies and probably reflected random associations. The knowledge of symbiotic microbiota in A. thunbergii will provide useful background information for controlling this devastating coffee plant pest.