Bumble bee parasite strains vary in resistance to phytochemicals

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Abstract

Nectar and pollen contain diverse phytochemicals that can reduce disease in pollinators. However, prior studies showed variable effects of nectar chemicals on infection, which could reflect variable phytochemical resistance among parasite strains. Inter-strain variation in resistance could influence evolutionary interactions between plants, pollinators, and pollinator disease, but testing direct effects of phytochemicals on parasites requires elimination of variation between bees. Using cell cultures of the bumble bee parasite Crithidia bombi, we determined (1) growth-inhibiting effects of nine floral phytochemicals and (2) variation in phytochemical resistance among four parasite strains. C. bombi growth was unaffected by naturally occurring concentrations of the known antitrypanosomal phenolics gallic acid, caffeic acid, and chlorogenic acid. However, C. bombi growth was inhibited by anabasine, eugenol, and thymol. Strains varied >3-fold in phytochemical resistance, suggesting that selection for phytochemical resistance could drive parasite evolution. Inhibitory concentrations of thymol (4.53–22.2 ppm) were similar to concentrations in Thymus vulgaris nectar (mean 5.2 ppm). Exposure of C. bombi to naturally occurring levels of phytochemicals—either within bees or during parasite transmission via flowers—could influence infection in nature. Flowers that produce antiparasitic phytochemicals, including thymol, could potentially reduce infection in Bombus populations, thereby counteracting a possible contributor to pollinator decline.

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The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen.

Violeta Sanchez, Sungbeom Lee, Christian Abel … (2012)

Flowers have a high risk of pathogen attack because of their rich nutrient and moisture content, and high frequency of insect visitors. We investigated the role of (E)-β-caryophyllene in floral defense against a microbial pathogen. This sesquiterpene is a common volatile compound emitted from flowers, and is a major volatile released from the stigma of Arabidopsis thaliana flowers. Arabidopsis thaliana lines lacking a functional (E)-β-caryophyllene synthase or constitutively overexpressing this gene were challenged with Pseudomonas syringae pv. tomato DC3000, which is a bacterial pathogen of brassicaceous plants. Flowers of plant lines lacking (E)-β-caryophyllene emission showed greater bacterial growth on their stigmas than did wild-type flowers, and their seeds were lighter and misshapen. By contrast, plant lines with ectopic (E)-β-caryophyllene emission from vegetative parts were more resistant than wild-type plants to pathogen infection of leaves, and showed reduced cell damage and higher seed production. Based on in vitro experiments, (E)-β-caryophyllene seems to act by direct inhibition of bacterial growth, rather than by triggering defense signaling pathways. (E)-β-Caryophyllene thus appears to serve as a defense against pathogens that invade floral tissues and, like other floral volatiles, may play multiple roles in defense and pollinator attraction. © 2011 The Authors. New Phytologist © 2011 New Phytologist Trust.

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Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order 'Enterobacteriales' of the Gammaproteobacteria.

Waldan Kwong, Nancy Moran (2013)

Gut-associated bacteria were isolated in axenic culture from the honey bee Apis mellifera and the bumble bees Bombus bimaculatus and B. vagans and are here placed in the novel genera and species Snodgrassella alvi gen. nov., sp. nov. and Gilliamella apicola gen. nov., sp. nov. Two strains from A. mellifera were characterized and are proposed as the type strains of Snodgrassella alvi (type strain wkB2(T) =NCIMB 14803(T) =ATCC BAA-2449(T) =NRRL B-59751(T)) and Gilliamella apicola (type strain wkB1(T) =NCIMB 14804(T) =ATCC BAA-2448(T)), representing, respectively, phylotypes referred to as 'Betaproteobacteria' and 'Gammaproteobacteria-1'/'Gamma-1' in earlier publications. These strains grew optimally under microaerophilic conditions, and did not grow readily under a normal atmosphere. The predominant fatty acids in both strains were palmitic acid (C16:0) and cis-vaccenic acid (C18:1ω7c and/or C18:1ω6c), and both strains had ubiquinone-8 as their major respiratory quinone. The DNA G+C contents were 41.3 and 33.6 mol% for wkB2(T) and wkB1(T), respectively. The Snodgrassella alvi strains from honey bees and bumble bees formed a novel clade within the family Neisseriaceae of the Betaproteobacteria, showing about 94% 16S rRNA gene sequence identity to their closest relatives, species of Stenoxybacter, Alysiella and Kingella. The Gilliamella apicola strains showed the highest 16S rRNA gene sequence identity to Orbus hercynius CN3(T) (93.9%) and several sequences from uncultured insect-associated bacteria. Phylogenetic reconstruction using conserved, single-copy amino acid sequences showed Gilliamella apicola as sister to the order 'Enterobacteriales' of the Gammaproteobacteria. Given its large sequence divergence from and basal position to the well-established order 'Enterobacteriales', we propose to place the clade encompassing Gilliamella apicola and O. hercynius in a new family and order, Orbaceae fam. nov. and Orbales ord. nov.

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Antitrypanosomal and antileishmanial activities of flavonoids and their analogues: in vitro, in vivo, structure-activity relationship, and quantitative structure-activity relationship studies.

Martin Schmidt, Vanessa Yardley, T Rüedi … (2006)

Trypanosomiasis and leishmaniasis are important parasitic diseases affecting millions of people in Africa, Asia, and South America. In a previous study, we identified several flavonoid glycosides as antiprotozoal principles from a Turkish plant. Here we surveyed a large set of flavonoid aglycones and glycosides, as well as a panel of other related compounds of phenolic and phenylpropanoid nature, for their in vitro activities against Trypanosoma brucei rhodesiense, Trypanosoma cruzi, and Leishmania donovani. The cytotoxicities of more than 100 compounds for mammalian L6 cells were also assessed and compared to their antiparasitic activities. Several compounds were investigated in vivo for their antileishmanial and antitrypanosomal efficacies in mouse models. Overall, the best in vitro trypanocidal activity for T. brucei rhodesiense was exerted by 7,8-dihydroxyflavone (50% inhibitory concentration [IC50], 68 ng/ml), followed by 3-hydroxyflavone, rhamnetin, and 7,8,3',4'-tetrahydroxyflavone (IC50s, 0.5 microg/ml) and catechol (IC50, 0.8 microg/ml). The activity against T. cruzi was moderate, and only chrysin dimethylether and 3-hydroxydaidzein had IC50s less than 5.0 microg/ml. The majority of the metabolites tested possessed remarkable leishmanicidal potential. Fisetin, 3-hydroxyflavone, luteolin, and quercetin were the most potent, giving IC50s of 0.6, 0.7, 0.8, and 1.0 microg/ml, respectively. 7,8-Dihydroxyflavone and quercetin appeared to ameliorate parasitic infections in mouse models. Generally, the test compounds lacked cytotoxicity in vitro and in vivo. By screening a large number of flavonoids and analogues, we were able to establish some general trends with respect to the structure-activity relationship, but it was not possible to draw clear and detailed quantitative structure-activity relationships for any of the bioactivities by two different approaches. However, our results can help in directing the rational design of 7,8-dihydroxyflavone and quercetin derivatives as potent and effective antiprotozoal agents.

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Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group

ISSN (Electronic): 2045-2322

Publication date (Electronic): 24 November 2016

Publication date Collection: 2016

Volume: 6

Electronic Location Identifier: 37087

Affiliations

[1 ]Department of Biology, University of Massachusetts at Amherst , Amherst, Massachusetts 01003, United States

[2 ]School of Biological Sciences, Illinois State University , Normal, Illinois 61790, United States

[3 ]Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE, United Kingdom

[4 ]University of Greenwich , Medway, ME4 4TB, United Kingdom

[5 ]Department of Applied Ecology, North Carolina State University , Raleigh, North Carolina 27695, United States

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[a ] ecp52@ 123456cornell.edu

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Publisher Item ID: srep37087

DOI: 10.1038/srep37087

PMC ID: 5121629

PubMed ID: 27883009

SO-VID: c60ec3fb-6764-4160-aa75-5b8141bb544a

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Bumble bee parasite strains vary in resistance to phytochemicals

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Most cited references 50

The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen.

Antitrypanosomal and antileishmanial activities of flavonoids and their analogues: in vitro, in vivo, structure-activity relationship, and quantitative structure-activity relationship studies.

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