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pH-mediated inhibition of a bumble bee parasite by an intestinal symbiont

Published online by Cambridge University Press:  24 September 2018

Evan C. Palmer-Young Open the ORCID record for Evan C. Palmer-Young [Opens in a new window] ,
Thomas R. Raffel  and
Quinn S. McFrederick
Evan C. Palmer-Young*
Affiliation:
Department of Entomology, University of California Riverside, Riverside, CA, USA
Thomas R. Raffel
Affiliation:
Department of Biology, Oakland University, Rochester, MI, USA
Quinn S. McFrederick
Affiliation:
Department of Entomology, University of California Riverside, Riverside, CA, USA
*
Author for correspondence: Evan C. Palmer-Young, E-mail: [email protected]
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Abstract

Gut symbionts can augment resistance to pathogens by stimulating host-immune responses, competing for space and nutrients, or producing antimicrobial metabolites. Gut microbiota of social bees, which pollinate many crops and wildflowers, protect hosts against diverse infections and might counteract pathogen-related bee declines. Bumble bee gut microbiota, and specifically abundance of Lactobacillus ‘Firm-5’ bacteria, can enhance resistance to the trypanosomatid parasite Crithidia bombi. However, the mechanism underlying this effect remains unknown. We hypothesized that the Firm-5 bacterium Lactobacillus bombicola, which produces lactic acid, inhibits C. bombi via pH-mediated effects. Consistent with our hypothesis, L. bombicola spent medium inhibited C. bombi growth via reduction in pH that was both necessary and sufficient for inhibition. Inhibition of all parasite strains occurred within the pH range documented in honey bees, though sensitivity to acidity varied among strains. Spent medium was slightly more potent than HCl, d- and l-lactic acids for a given pH, suggesting that other metabolites also contribute to inhibition. Results implicate symbiont-mediated reduction in gut pH as a key determinant of trypanosomatid infection in bees. Future investigation into in vivo effects of gut microbiota on pH and infection intensity would test the relevance of these findings for bees threatened by trypanosomatids.

Keywords

Cell-free supernatantcompetitionFirmicutesflagellateslactic acid bacteriamicrobiomeparasite strain variationpH-dependent interactionspollinator declineTrypanosomatidae
Type
Research Article
Information
Parasitology , Volume 146 , Issue 3 , March 2019 , pp. 380 - 388
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Copyright
Copyright © Cambridge University Press 2018 

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References

Adams, MR and Hall, CJ (1988) Growth inhibition of food-borne pathogens by lactic and acetic acids and their mixtures. International Journal of Food Science & Technology 23, 287–292.Google Scholar
Anderson, KE, Carroll, MJ, Sheehan, T, Mott, BM, Maes, P and Corby-Harris, V (2014) Hive-stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Molecular Ecology 23, 5904–5917.Google Scholar
Barribeau, SM, Sadd, BM, du Plessis, L and Schmid-Hempel, P (2014) Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system. Proceedings of the National Academy of Sciences 111, 3496–3501.Google Scholar
Benthin, S and Villadsen, J (1995) Different inhibition of Lactobacillus delbrueckii subsp. bulgaricus by d- and l-lactic acid: effects on lag phase, growth rate and cell yield. Journal of Applied Bacteriology 78, 647–654.Google Scholar
Billiet, A, Meeus, I, Van Nieuwerburgh, F, Deforce, D, Wäckers, F and Smagghe, G (2017) Colony contact contributes to the diversity of gut bacteria in bumblebees (Bombus terrestris). Insect Science 24, 270–277.Google Scholar
Bringaud, F, Rivière, L and Coustou, V (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Molecular and Biochemical Parasitology 149, 1–9.Google Scholar
Brown, MJF, Schmid-Hempel, R and Schmid-Hempel, P (2003) Strong context-dependent virulence in a host–parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology 72, 994–1002.Google Scholar
Cameron, SA, Lozier, JD, Strange, JP, Koch, JB, Cordes, N, Solter, LF and Griswold, TL (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences 108, 662–667.Google Scholar
Cariveau, DP, Elijah Powell, J, Koch, H, Winfree, R and Moran, NA (2014) Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). The ISME Journal 8, 2369–2379.Google Scholar
Cornman, RS, Tarpy, DR, Chen, Y, Jeffreys, L, Lopez, D, Pettis, JS, vanEngelsdorp, D and Evans, JD (2012) Pathogen webs in collapsing honey bee colonies. PLoS ONE 7, e43562.Google Scholar
Cox, AJ, Pyne, DB, Saunders, PU and Fricker, PA (2010) Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes. British Journal of Sports Medicine 44, 222–226.Google Scholar
Daskin, JH, Bell, SC, Schwarzkopf, L and Alford, RA (2014) Cool temperatures reduce antifungal activity of symbiotic bacteria of threatened amphibians – implications for disease management and patterns of decline. PLoS ONE 9, e100378.Google Scholar
De Keersmaecker, SCJ, Verhoeven, TLA, Desair, J, Marchal, K, Vanderleyden, J and Nagy, I (2006) Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiology Letters 259, 89–96.Google Scholar
Dillon, RJ and Dillon, VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annual Review of Entomology 49, 71–92.Google Scholar
Engel, P, Martinson, VG and Moran, NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences 109, 11002–11007.Google Scholar
Engel, P, Kwong, WK, McFrederick, Q, Anderson, KE, Barribeau, SM, Chandler, JA, Cornman, RS, Dainat, J, Miranda, JR, de, Doublet, V, Emery, O, Evans, JD, Farinelli, L, Flenniken, ML, Granberg, F, Grasis, JA, Gauthier, L, Hayer, J, Koch, H, Kocher, S, Martinson, VG, Moran, N, Munoz-Torres, M, Newton, I, Paxton, RJ, Powell, E, Sadd, BM, Schmid-Hempel, P, Schmid-Hempel, R, Song, SJ, Schwarz, RS, vanEngelsdorp, D and Dainat, B (2016) The bee microbiome: impact on bee health and model for evolution and ecology of host–microbe interactions. mBio 7, e02164–15.Google Scholar
Evans, JD and Armstrong, T-N (2006) Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecology 6, 4.Google Scholar
Evans, JD and Lopez, DL (2004) Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 97, 752–756.Google Scholar
Evans, JD and Spivak, M (2010) Socialized medicine: individual and communal disease barriers in honey bees. Journal of Invertebrate Pathology 103(Suppl.), S62–S72.Google Scholar
Ewaschuk, JB, Zello, GA, Naylor, JM and Brocks, DR (2002) Metabolic acidosis: separation methods and biological relevance of organic acids and lactic acid enantiomers. Journal of Chromatography B 781, 39–56.Google Scholar
Fauser-Misslin, A, Sadd, BM, Neumann, P and Sandrock, C (2014) Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. Journal of Applied Ecology 51, 450–459.Google Scholar
Fayol-Messaoudi, D, Berger, CN, Coconnier-Polter, M-H, Moal, VL-L and Servin, AL (2005) pH-, lactic acid-, and non-lactic acid-dependent activities of probiotic Lactobacilli against Salmonella enterica serovar Typhimurium. Applied and Environmental Microbiology 71, 6008–6013.Google Scholar
Forsgren, E, Olofsson, TC, Váasquez, A and Fries, I (2010) Novel lactic acid bacteria inhibiting Paenibacillus larvae. Apidologie 41, 99–108.Google Scholar
Fürst, MA, McMahon, DP, Osborne, JL, Paxton, RJ and Brown, MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366.Google Scholar
Gaggìa, F, Baffoni, L and Alberoni, D (2018) Probiotics for honeybees’ health. In Di Gioia D and Biavati B (eds), Probiotics and Prebiotics in Animal Health and Food Safety. Cham: Springer, pp. 219–245. doi: 10.1007/978-3-319-71950-4_9.Google Scholar
Gallai, N, Salles, J-M, Settele, J and Vaissière, BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68, 810–821.Google Scholar
Gegear, RJ, Otterstatter, MC and Thomson, JD (2005) Does parasitic infection impair the ability of bumblebees to learn flower-handling techniques? Animal Behaviour 70, 209–215.Google Scholar
Gegear, RJ, Otterstatter, MC and Thomson, JD (2006) Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of Biological Sciences/The Royal Society 273, 1073–1078.Google Scholar
Glass, KA, Loeffelholz, JM, Ford, JP and Doyle, MP (1992) Fate of Escherichia coli O157:H7 as affected by pH or sodium chloride and in fermented, dry sausage. Applied and Environmental Microbiology 58, 2513–2516.Google Scholar
Gorbach, SL (1990) Lactic acid bacteria and human health. Annals of Medicine 22, 37–41.Google Scholar
Gorbunov, PS (1996) Peculiarities of life cycle in flagellate Crithidia bombi (protozoa, trypanosomatidae). Zoologicheskii Zhurnal 75, 808–810.Google Scholar
Goulson, D, Nicholls, E, Botías, C and Rotheray, EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957.Google Scholar
Graystock, P, Blane, EJ, McFrederick, QS, Goulson, D and Hughes, WOH (2016) Do managed bees drive parasite spread and emergence in wild bees? International Journal for Parasitology: Parasites and Wildlife 5, 64–75.Google Scholar
Imhoof, B and Schmid-Hempel, P (1998) Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117, 331–336.Google Scholar
Kamada, N, Chen, GY, Inohara, N and Núñez, G (2013) Control of pathogens and pathobionts by the gut microbiota. Nature Immunology 14, 685–690.Google Scholar
Kešnerová, L, Mars, RAT, Ellegaard, KM, Troilo, M, Sauer, U and Engel, P (2017) Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biology 15, e2003467.Google Scholar
Klein, A-M, Vaissière, BE, Cane, JH, Steffan-Dewenter, I, Cunningham, S, Kremen, C and Tscharntke, T (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274, 303–313.Google Scholar
Koch, H and Schmid-Hempel, P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences of the United States of America 108, 19288–19292.Google Scholar
Koch, H and Schmid-Hempel, P (2012) Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host–parasite system. Ecology Letters 15, 1095–1103.Google Scholar
Koch, H, Cisarovsky, G and Schmid-Hempel, P (2012) Ecological effects on gut bacterial communities in wild bumblebee colonies. The Journal of Animal Ecology 81, 1202–1210.Google Scholar
Kwong, WK and Moran, NA (2013) 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. International Journal of Systematic and Evolutionary Microbiology 63, 2008–2018.Google Scholar
Kwong, WK and Moran, NA (2016) Gut microbial communities of social bees. Nature Reviews Microbiology 14, 374–384.Google Scholar
Kwong, WK, Mancenido, AL and Moran, NA (2017 a) Immune system stimulation by the native gut microbiota of honey bees. Open Science 4, 170003.Google Scholar
Kwong, WK, Medina, LA, Koch, H, Sing, K-W, Soh, EJY, Ascher, JS, Jaffé, R and Moran, NA (2017 b) Dynamic microbiome evolution in social bees. Science Advances 3, e1600513.Google Scholar
Li, J, Powell, JE, Guo, J, Evans, JD, Wu, J, Williams, P, Lin, Q, Moran, NA and Zhang, Z (2015) Two gut community enterotypes recur in diverse bumblebee species. Current Biology 25, R652–R653.Google Scholar
Lindgren, SE and Dobrogosz, WJ (1990) Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiology Letters 87, 149–164.Google Scholar
Martinson, VG, Danforth, BN, Minckley, RL, Rueppell, O, Tingek, S and Moran, NA (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20, 619–628.Google Scholar
McMahon, DP, Fürst, MA, Caspar, J, Theodorou, P, Brown, MJF and Paxton, RJ (2015) A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. Journal of Animal Ecology 84, 615–624.Google Scholar
Mockler, BK, Kwong, WK, Moran, NA and Koch, H (2018) Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Applied and Environmental Microbiology 84, e02335–17.Google Scholar
Morton, JT, Sanders, J, Quinn, RA, McDonald, D, Gonzalez, A, Vázquez-Baeza, Y, Navas-Molina, JA, Song, SJ, Metcalf, JL, Hyde, ER, Lladser, M, Dorrestein, PC and Knight, R (2017) Balance trees reveal microbial niche differentiation. mSystems 2, e00162–16.Google Scholar
Mueller, UG and Sachs, JL (2015) Engineering microbiomes to improve plant and animal health. Trends in Microbiology 23, 606–617.Google Scholar
Palmer-Young, EC, Sadd, BM, Stevenson, PC, Irwin, RE and Adler, LS (2016) Bumble bee parasite strains vary in resistance to phytochemicals. Scientific Reports 6, 37087.Google Scholar
Palmer-Young, EC, Sadd, BM, Irwin, RE and Adler, LS (2017 a) Synergistic effects of floral phytochemicals against a bumble bee parasite. Ecology and Evolution 7, 1836–1849.Google Scholar
Palmer-Young, EC, Hogeboom, A, Kaye, AJ, Donnelly, D, Andicoechea, J, Connon, SJ, Weston, I, Skyrm, K, Irwin, RE and Adler, LS (2017 b) Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees. PLoS ONE 12, e0183729.Google Scholar
Praet, J, Meeus, I, Cnockaert, M, Houf, K, Smagghe, G and Vandamme, P (2015) Novel lactic acid bacteria isolated from the bumble bee gut: Convivina intestini gen. nov., sp. nov., Lactobacillus bombicola sp. nov., and Weissella bombi sp. nov. Antonie van Leeuwenhoek 107, 1337–1349.Google Scholar
Praet, J, Parmentier, A, Schmid-Hempel, R, Meeus, I, Smagghe, G and Vandamme, P (2018) Large-scale cultivation of the bumblebee gut microbiota reveals an underestimated bacterial species diversity capable of pathogen inhibition. Environmental Microbiology 20, 214–227.Google Scholar
Presser, KA, Ratkowsky, DA and Ross, T (1997) Modelling the growth rate of Escherichia coli as a function of pH and lactic acid concentration. Applied and Environmental Microbiology 63, 2355–2360.Google Scholar
R Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Ratzke, C and Gore, J (2018) Modifying and reacting to the environmental pH can drive bacterial interactions. PLoS Biology 16, e2004248.Google Scholar
Ravoet, J, Maharramov, J, Meeus, I, De Smet, L, Wenseleers, T, Smagghe, G and de Graaf, DC (2013) Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS ONE 8, e72443.Google Scholar
Raymann, K and Moran, NA (2018) The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science 26, 97–104.Google Scholar
Ritz, C, Baty, F, Streibig, JC and Gerhard, D (2015) Dose-response analysis using R. PLoS ONE 10, e0146021.Google Scholar
Round, JL and Mazmanian, SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nature Reviews Immunology 9, 313–323.Google Scholar
Runckel, C, DeRisi, J and Flenniken, ML (2014) A draft genome of the honey bee trypanosomatid parasite Crithidia mellificae. PLOS ONE 9, e95057.Google Scholar
Russell, JB and Diez-Gonzalez, F (1998) The effects of fermentation acids on bacterial growth. Advances in Microbial Physiology 39, 205–234.Google Scholar
Sabaté, DC, Carrillo, L and Carina Audisio, M (2009) Inhibition of Paenibacillus larvae and Ascosphaera apis by Bacillus subtilis isolated from honeybee gut and honey samples. Research in Microbiology 160, 193–199.Google Scholar
Sadd, BM (2011) Food-environment mediates the outcome of specific interactions between a bumblebee and its trypanosome parasite. Evolution 65, 2995–3001.Google Scholar
Salathé, R, Tognazzo, M, Schmid-Hempel, R and Schmid-Hempel, P (2012) Probing mixed-genotype infections I: extraction and cloning of infections from hosts of the trypanosomatid Crithidia bombi. PLoS ONE 7, e49046.Google Scholar
Salminen, S and von Wright, A (2004) Lactic Acid Bacteria: Microbiological and Functional Aspects, 3rd Edn. Boca Raton, FL: CRC Press.Google Scholar
Schmid-Hempel, P and Ebert, D (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution 18, 27–32.Google Scholar
Schmid-Hempel, R, Eckhardt, M, Goulson, D, Heinzmann, D, Lange, C, Plischuk, S, Escudero, LR, Salathé, R, Scriven, JJ and Schmid-Hempel, P (2014) The invasion of Southern South America by imported bumblebees and associated parasites. Journal of Animal Ecology 83, 823–837.Google Scholar
Schwarz, RS, Bauchan, GR, Murphy, CA, Ravoet, J, de Graaf, DC and Evans, JD (2015) Characterization of two species of trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, and Lotmaria passim n. gen., n. sp. Journal of Eukaryotic Microbiology 62, 567–583.Google Scholar
Schwarz, RS, Moran, NA and Evans, JD (2016) Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proceedings of the National Academy of Sciences 113, 9345–9350.Google Scholar
Scrimshaw, NS, Taylor, CE and Gordon, JE (1959) Interactions of nutrition and infection. American Journal of Medical Sciences 237, 367–403.Google Scholar
Shykoff, JA and Schmid-Hempel, P (1991) Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie 22, 117–125.Google Scholar
Stark, CM and Nylund, CM (2016) Side effects and complications of proton pump inhibitors: a pediatric perspective. The Journal of Pediatrics 168, 16–22.Google Scholar
Steele, MI, Kwong, WK, Whiteley, M and Moran, NA (2017) Diversification of type VI secretion system toxins reveals ancient antagonism among bee gut microbes. mBio 8, e01630–17.Google Scholar
Tripodi, AD, Szalanski, AL and Strange, JP (2018) Novel multiplex PCR reveals multiple trypanosomatid species infecting North American bumble bees (Hymenoptera: Apidae: Bombus). Journal of Invertebrate Pathology 153, 147–155.Google Scholar
Vásquez, A, Forsgren, E, Fries, I, Paxton, RJ, Flaberg, E, Szekely, L and Olofsson, TC (2012) Symbionts as Major modulators of insect health: lactic acid Bacteria and honeybees. PLoS ONE 7, e33188.Google Scholar
Zheng, H, Powell, JE, Steele, MI, Dietrich, C and Moran, NA (2017) Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings of the National Academy of Sciences 114, 4775–4780.Google Scholar
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