Bacterial Communities of Two Parthenogenetic Aphid Species Cocolonizing Two Host Plants across the Hawaiian Islands

Jones, Ryan; Bressan, Alberto; Greenwell, April M.; Fierer, Noah

doi:10.1128/aem.05974-11

Cited by 59 publications

(64 citation statements)

References 35 publications

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“…Wolbachia has indeed only been detected in 22 aphid species so far, with prevalence values ranging between 0.4 and 100% within species (Wang et al 2009, Augustinos et al 2011, Jones et al 2011.…”

Section: Discussionmentioning

confidence: 95%

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Combination of Genomic and Proteomic Approaches to Characterize the Symbiotic Population of the Banana Aphid (Hemiptera: Aphididae)

et al. 2014

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Aphids are known to live in symbiosis with specific bacteria called endosymbionts that have positive or negative impacts on their hosts. In this study, six banana aphid (Pentalonia nigronervosa Coquerel) strains from various geographical origins (Gabon, Madagascar, and Burundi) were screened to determine their symbiotic content, using complementary genomic (16S rDNA sequencing and specific polymerase chain reaction) and proteomic (two-dimensional difference gel electrophoresis coupled with protein identification by matrix-assisted laser desorption-ionization time-of-flight mass spectrometry) approaches. Despite the geographical heterogeneity, the combined methods allowed us to identify the same two symbionts in the six aphids strains tested: Buchnera aphidicola and Wolbachia. Although B. aphidicola is found in almost all aphid species, the systematic presence of Wolbachia in banana aphids is particularly interesting, as this bacterium usually has a low prevalence in aphid species. Phylogenetic analyses showed that the Wolbachia sp. strain found in P. nigronervosa was very similar to the strain present in aphids of the genus Cinara, known to have developed a strong and long-term symbiotic association with Wolbachia. The high level of asexual reproduction in P. nigronervosa could be linked to the presence of Wolbachia, but its prevalence also suggests that this symbiotic bacterium could play a more essential role in its aphid host.

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Section: Discussionmentioning

confidence: 95%

“…fact that a nearly systematic occurrence of Wolbachia was recorded in another aphid species of the genus Pentalonia (Pentalonia caladii [Hemiptera: Aphididae]) in Hawaii (Jones et al 2011).…”

Section: Discussionmentioning

confidence: 99%

Combination of Genomic and Proteomic Approaches to Characterize the Symbiotic Population of the Banana Aphid (Hemiptera: Aphididae)

et al. 2014

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“…This aphid harbors the obligate endosymbiont Buchnera, while the facultative bacteria found commonly in the pea aphid and related species, such as Regiella insecticola, H. defensa, and S. symbiotica, are absent or rare (32)(33)(34). The taxon Aphis gossypii (like the pea aphid) is composed of a series of host plant races or biotypes that are to various degrees specialized on different host plant groups.…”

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confidence: 99%

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

Zhang

Cao

Zhong

et al. 2016

Appl Environ Microbiol

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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 ...

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“…In the perspective of basic research, additional study may focus on the cellular mechanisms that are involved in the internalization of BBTV viral particles through the epithelial tissues (AMG and PSGs) of the aphid vectors, and on the possible interaction of BBTV with GroELs proteins produced by endosymbiotic bacteria that are harboured in Pentalonia aphids haemocoel [53]. …”

Section: Resultsmentioning

confidence: 99%

Localization, Concentration, and Transmission Efficiency of Banana bunchy top virus in Four Asexual Lineages of Pentalonia aphids

Watanabe

Greenwell

Bressan

2013

Viruses

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Banana bunchy top virus (BBTV) is the most destructive pathogenic virus of banana plants worldwide. The virus is transmitted in a circulative non-propagative manner by the banana aphid, Pentalonia nigronervosa Coquerel. In this work, we examined the localization, accumulation, and transmission efficiency of BBTV in four laboratory-established lineages of Pentalonia aphids derived from four different host plants: taro (Colocasia esculenta), heliconia (Heliconia spp.), red ginger (Alpinia purpurata), and banana (Musa sp.). Mitochondrial sequencing identified three and one lineages as Pentalonia caladii van der Goot, a recently proposed species, and P. nigronervosa, respectively. Microsatellite analysis separated the aphid lineages into four distinct genotypes. The transmission of BBTV was tested using leaf disk and whole-plant assays, both of which showed that all four lineages are competent vectors of BBTV, although the P. caladii from heliconia transmitted BBTV to the leaf disks at a significantly lower rate than did P. nigronervosa. The concentration of BBTV in dissected guts, haemolymph, and salivary glands was quantified by real-time PCR. The BBTV titer reached similar concentrations in the guts, haemolymph, and salivary glands of aphids from all four lineages tested. Furthermore, immunofluorescence assays showed that BBTV antigens localized to the anterior midguts and the principal salivary glands, demonstrating a similar pattern of translocations across the four lineages. The results reported in this study showed for the first time that P. caladii is a competent vector of BBTV.

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Bacterial Communities of Two Parthenogenetic Aphid Species Cocolonizing Two Host Plants across the Hawaiian Islands

Cited by 59 publications

References 35 publications

Combination of Genomic and Proteomic Approaches to Characterize the Symbiotic Population of the Banana Aphid (Hemiptera: Aphididae)

Combination of Genomic and Proteomic Approaches to Characterize the Symbiotic Population of the Banana Aphid (Hemiptera: Aphididae)

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

Localization, Concentration, and Transmission Efficiency of Banana bunchy top virus in Four Asexual Lineages of Pentalonia aphids

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