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Amphibian Host and Skin Microbiota Response to a Common Agricultural Antimicrobial and Internal Parasite

Microbial Ecology volume 79, pages 175–191 (2020)Cite this article

Abstract

Holistic approaches that simultaneously characterize responses of both microbial symbionts and their hosts to environmental shifts are imperative to understanding the role of microbiotas on host health. Using the northern leopard frog (Lithobates pipiens) as our model, we investigated the effects of a common trematode (family Echinostomatidae), a common agricultural antimicrobial (Sulfadimethoxine; SDM), and their interaction on amphibian skin microbiota and amphibian health (growth metrics and susceptibility to parasites). In the trematode-exposed individuals, we noted an increase in alpha diversity and a shift in microbial communities. In the SDM-treated individuals, we found a change in the composition of the skin microbiota similar to those induced by the trematode treatment. Groups treated with SDM, echinostomes, or a combination of SDM and echinostomes, had higher relative abundances of OTUs assigned to Flavobacterium and Acinetobacter. Both of these genera have been associated with infectious disease in amphibians and the production of anti-pathogen metabolites. Similar changes in microbial community composition between SDM and trematode exposed individuals may have resulted from stress-related disruption of host immunity. Despite changes in the microbiota, we found no effect of echinostomes and SDM on host health. Given the current disease- and pollution-related threats facing amphibians, our study highlights the need to continue to evaluate the influence of natural and anthropogenic stressors on host-associated microbial communities.

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References

  1. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336:1255–1262. https://doi.org/10.1126/science.1224203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Grice EA, Segre JA (2012) The human microbiome: our second genome. Annu Rev Genomics Hum Genet 13:151–170. https://doi.org/10.1146/annurev-genom-090711-163814

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Kaplan JL, Shi HN, Walker WA (2011) The role of microbes in developmental immunologic programming. Pediatr Res 69:465–472. https://doi.org/10.1203/PDR.0b013e318217638a

    Article  PubMed  Google Scholar 

  4. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810. https://doi.org/10.1038/nature06244

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Cho I, Blaser MJ (2012) The human microbiome: at the Interface of health and disease. Nat Rev Genet 13:260–270. https://doi.org/10.1038/nrg3182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Jani AJ, Briggs CJ (2014) The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proc Natl Acad Sci U S A 111:E5049–E5058. https://doi.org/10.1073/pnas.1412752111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Soen Y (2014) Environmental disruption of host-microbe co-adaptation as a potential driving force in evolution. Front Genet 5:168. https://doi.org/10.3389/fgene.2014.00168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, Kremer M, Chaffron S, Macpherson AJ, Buer J, Parkhill J, Dougan G, von Mering C, Hardt W-D (2007) Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5:2177–2189. https://doi.org/10.1371/journal.pbio.0050244

    Article  PubMed  CAS  Google Scholar 

  9. Petersen C, Round JL (2014) Defining Dysbiosis and its influence on host immunity and disease. Cell Microbiol 16:1024–1033. https://doi.org/10.1111/cmi.12308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Berendsen RL, Pieterse CMJ, Bakker P (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001

    Article  PubMed  CAS  Google Scholar 

  11. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woodhams DC, Briggs CJ, Vredenburg VT, Minbiole KPC (2009) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3:818–824. https://doi.org/10.1038/ismej.2009.27

    Article  PubMed  CAS  Google Scholar 

  12. Stecher B, Hardt WD (2008) The role of microbiota in infectious disease. Trends Microbiol 16:107–114. https://doi.org/10.1016/j.tim.2007.12.008

    Article  PubMed  CAS  Google Scholar 

  13. Brown SP, Inglis RF, Taddei F (2009) Evolutionary ecology of microbial wars: within-host competition and (incidental) virulence. Evol Appl 2:32–39. https://doi.org/10.1111/j.1752-4571.2008.00059.x

    Article  PubMed  PubMed Central  Google Scholar 

  14. Dheilly NM, Poulin R, Thomas F (2015) Biological warfare: microorganisms as drivers of host-parasite interactions. Infect Genet Evol 34:251–259. https://doi.org/10.1016/j.meegid.2015.05.027

    Article  PubMed  Google Scholar 

  15. Boutin S, Bernatchez L, Audet C, Derome N (2013) Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS One 8:e84772. https://doi.org/10.1371/journal.pone.0084772

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Kelly C, Salinas I (2017) Under pressure: interactions between commensal microbiota and the teleost immune system. Front Immunol 8:559. https://doi.org/10.3389/fimmu.2017.00559

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Dietrich JP, Van Gaest AL, Strickland SA, Arkoosh MR (2014) The impact of temperature stress and pesticide exposure on mortality and disease susceptibility of endangered Pacific Salmon. Chemosphere 108:353–359. https://doi.org/10.1016/j.chemosphere.2014.01.079

    Article  PubMed  CAS  Google Scholar 

  18. Doublet V, Labarussias M, de Miranda JR, Moritz RFA, Paxton RJ (2015) Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ Microbiol 17:969–983. https://doi.org/10.1111/1462-2920.12426

    Article  PubMed  CAS  Google Scholar 

  19. Hua J, Wuerthner VP, Jones DK, Mattes B, Cothran RD, Relyea RA, Hoverman JT (2017) Evolved pesticide tolerance influences susceptibility to parasites in amphibians. Evol Appl 10:802–812. https://doi.org/10.1111/eva.12500

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. De Liguoro M, Poltronieri C, Capolongo F, Montesissa C (2007) Use of Sulfadimethoxine in intensive calf farming: evaluation of transfer to stable manure and soil. Chemosphere 68:671–676. https://doi.org/10.1016/j.chemosphere.2007.02.009

    Article  PubMed  CAS  Google Scholar 

  21. Becker MH, Harris RN (2010) Cutaneous bacteria of the redback salamander prevent morbidity associated with a lethal disease. PLoS One 5:e10957. https://doi.org/10.1371/journal.pone.0010957

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Colombo BM, Scalvenzi T, Benlamara S, Pollet N (2015) Microbiota and mucosal immunity in amphibians. Front Immunol 6. https://doi.org/10.3389/fimmu.2015.00111

  23. Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 5:735–748. https://doi.org/10.3201/eid0506.990601

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Becker MH, Walke JB, Murrill L, Woodhams DC, Reinert LK, Rollins-Smith LA, Burzynski EA, Umile TP, Minbiole KPC, Belden LK (2015) Phylogenetic distribution of symbiotic bacteria from Panamanian amphibians that inhibit growth of the lethal fungal pathogen Batrachochytrium dendrobatidis. Mol Ecol 24:1628–1641. https://doi.org/10.1111/mec.13135

    Article  PubMed  Google Scholar 

  25. Johnson PTJ, McKenzie VJ (2009) Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America. In: Toledo R, Fried B (eds) The biology of Echinostomes. Springer, New York, pp 249–280

    Chapter  Google Scholar 

  26. Martin TR, Conn DB (1990) The pathogenicity, localization, and cyst structure of Echinostomatid Metacercariae (Trematoda) infecting the kidneys of the frogs Rana clamitans and Rana pipiens. J Parasitol 76:414–419. https://doi.org/10.2307/3282677

    Article  PubMed  CAS  Google Scholar 

  27. Hoverman JT, Mihaljevic JR, Richgels KLD, Kerby JL, Johnson PTJ (2012) Widespread co-occurrence of virulent pathogens within California amphibian communities. Ecohealth 9:288–292. https://doi.org/10.1007/s10393-012-0778-2

    Article  PubMed  Google Scholar 

  28. Wuerthner VP, Hua J, Hoverman JT (2017) The benefits of coinfection: trematodes alter disease outcomes associated with virus infection. J Anim Ecol 86:921–931. https://doi.org/10.1111/1365-2656.12665

    Article  PubMed  Google Scholar 

  29. Reid KM, Patel S, Robinson AJ, Bu LJ, Jarungsriapisit J, Moore LJ, Salinas I (2017) Salmonid alphavirus infection causes skin Dysbiosis in Atlantic Salmon (Salmo salar L.) Post-smolts. PLoS One 12. https://doi.org/10.1371/journal.pone.0172856

    Article  CAS  Google Scholar 

  30. Jimenez RR, Sommer S (2017) The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers Conserv 26:763–786. https://doi.org/10.1007/s10531-016-1272-x

    Article  Google Scholar 

  31. Costa S, Lopes I, Proenca DN, Ribeiro R, Morais PV (2016) Diversity of cutaneous microbiome of Pelophylax perezi populations inhabiting different environments. Sci Total Environ 572:995–1004. https://doi.org/10.1016/j.scitotenv.2016.07.230

    Article  PubMed  CAS  Google Scholar 

  32. Koprivnikar J, Forbes MR, Baker RL (2007) Contaminant effects on host-parasite interactions: atrazine, frogs, and trematodes. Environ Toxicol Chem 26:2166–2170. https://doi.org/10.1897/07-220.1

    Article  PubMed  CAS  Google Scholar 

  33. Pochini KM, Hoverman JT (2017) Immediate and lag effects of pesticide exposure on parasite resistance in larval amphibians. Parasitology 144:817–822. https://doi.org/10.1017/s0031182016002560

    Article  PubMed  CAS  Google Scholar 

  34. Buss N, Hua J (2018) Parasite susceptibility in an amphibian host is modified by salinization and predators. Environ Pollut 236:754–763. https://doi.org/10.1016/j.envpol.2018.01.060

    Article  PubMed  CAS  Google Scholar 

  35. Rohr JR, Raffel TR, Sessions SK, Hudson PJ (2008) Understanding the net effects of pesticides on amphibian trematode infections. Ecol Appl 18:1743–1753. https://doi.org/10.1890/07-1429.1

    Article  PubMed  Google Scholar 

  36. Crisol-Martinez E, Moreno-Moyano LT, Wilkinson N, Prasai T, Brown PH, Moore RJ, Stanley D (2016) A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica). Peerj 4:e2002. https://doi.org/10.7717/peerj.2002

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287:443–449. https://doi.org/10.1126/science.287.5452.443

    Article  PubMed  CAS  Google Scholar 

  38. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652. https://doi.org/10.1038/nature09575

    Article  PubMed  CAS  Google Scholar 

  39. Dietze JE, Scribner EA, Meyer MT, Kolpin DW (2005) Occurrence of antibiotics in water from 13 Fish hatcheries, 2001-2003. Int J Environ Anal Chem 85:1141–1152. https://doi.org/10.1080/03067310500273682

    Article  CAS  Google Scholar 

  40. Llewellyn MS, Leadbeater S, Garcia C, Sylvain FE, Custodio M, Ang KP, Powell F, Carvalho GR, Creer S, Elliot J, Derome N (2017) Parasitism perturbs the mucosal microbiome of Atlantic Salmon. Sci Rep 7. https://doi.org/10.1038/srep43465

  41. Woodhams DC, Geiger CC, Reinert LK, Rollins-Smith LA, Lam B, Harris RN, Briggs CJ, Vredenburg VT, Voyles J (2012) Treatment of amphibians infected with Chytrid fungus: learning from failed trials with itraconazole, antimicrobial peptides, bacteria, and heat therapy. Dis Aquat Org 98:11–25. https://doi.org/10.3354/dao02429

    Article  PubMed  CAS  Google Scholar 

  42. Appelgate J (1983) Clinical-pharmacology of sulfonamides. Mod Vet Pract 64:667–669

    Google Scholar 

  43. Giguere S, Prescott JF, Dowling PM (2013) Antimicrobial therapy in veterinary medicine 5th edn. Wiley-Blackwell, Hoboken

    Book  Google Scholar 

  44. Bourne DWA, Bialer M, Dittert LW, Hayashi M, Rudawsky G, Koritz GD, Bevill RF (1981) Disposition of sulfadimethoxine in cattle-inclusion of protein-binding factors in a pharmacokinetic model. J Pharm Sci 70:1068–1072. https://doi.org/10.1002/jps.2600700926

    Article  PubMed  CAS  Google Scholar 

  45. Hamscher G, Priess B, Nau H (2006) A survey of the occurrence of various sulfonamides and tetracyclines in water and sediment samples originating from aquaculture systems in Northern Germany in summer 2005. Arch Leb 57:97–101

    CAS  Google Scholar 

  46. Kreuzig R, Holtge S, Brunotte J, Berenzen N, Wogram J, Schulz R (2005) Test-plot studies on runoff of sulfonamides from manured soils after sprinkler irrigation. Environ Toxicol Chem 24:777–781. https://doi.org/10.1897/04-019r.1

    Article  PubMed  CAS  Google Scholar 

  47. Kuchta SL, Cessna AJ, Elliott JA, Peru KM, Headley JV (2009) Transport of Lincomycin to surface and ground water from manure-amended cropland. J Environ Qual 38:1719–1727. https://doi.org/10.2134/jeq2008.0365

    Article  PubMed  CAS  Google Scholar 

  48. Kumar A, Schweizer HP (2005) Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv Drug Deliv Rev 57:1486–1513. https://doi.org/10.1016/j.addr.2005.04.004

    Article  PubMed  CAS  Google Scholar 

  49. Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759. https://doi.org/10.1016/j.chemosphere.2006.03.026

    Article  PubMed  CAS  Google Scholar 

  50. Huffman JE, Fried B (2012) The biology of Echinoparyphium (Trematoda, Echinostomatidae). Acta Parasitol 57:199–210. https://doi.org/10.2478/s11686-012-0042-5

    Article  PubMed  Google Scholar 

  51. Kanev I, Sterner M, Radev V, Fried B (2000) An overview of the biology of echinostomes. In: Fried B, Graczyk TK (eds) Echinostomes as experimental models for biological research. Springer, Dordrecht, pp 1–29

    Google Scholar 

  52. Schell SC (1985) Handbook of the trematodes of North America north of Mexico. University Press of Idaho, Moscow

    Google Scholar 

  53. Smyth JD, Halton DW (1983) The physiology of trematodes 2nd edn. Cambridge University Press, New York

    Google Scholar 

  54. Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions: 1. Regulatory Processes. J Anim Ecol 47:219–247. https://doi.org/10.2307/3933

    Article  Google Scholar 

  55. Gervasi SS, Stephens PR, Hua J, Searle CL, Xie GY, Urbina J, Olson DH, Bancroft BA, Weis V, Hammond JI, Relyea RA, Blaustein AR (2017) Linking ecology and epidemiology to understand predictors of multi-host responses to an emerging pathogen, the amphibian Chytrid fungus. PLoS One 12:e0167882. https://doi.org/10.1371/journal.pone.0167882

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Walke JB, Becker MH, Loftus SC, House LL, Teotonio TL, Minbiole KPC, Belden LK (2015) Community structure and function of amphibian skin microbes: an experiment with bullfrogs exposed to a Chytrid fungus. PLoS One 10. https://doi.org/10.1371/journal.pone.0139848

    Article  CAS  Google Scholar 

  57. Culp CE, Falkinham III JO, Belden LK (2007) Identification of the natural bacterial microflora on the skin of eastern newts, bullfrog tadpoles and Redback salamanders. Herpetologica 63:66–71. https://doi.org/10.1655/0018-0831(2007)63[66:iotnbm]2.0.co;2

    Article  Google Scholar 

  58. McKenzie VJ, Bowers RM, Fierer N, Knight R, Lauber CL (2012) Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME J 6:588–596. https://doi.org/10.1038/ismej.2011.129

    Article  PubMed  CAS  Google Scholar 

  59. LaFonte BE, Johnson PTJ (2013) Experimental infection dynamics: using immunosuppression and In Vivo parasite tracking to understand host resistance in an amphibian-trematode system. J Exp Biol 216:3700–3708. https://doi.org/10.1242/jeb.088104

    Article  PubMed  Google Scholar 

  60. Holland MP, Skelly DK, Kashgarian M, Bolden SR, Harrison LM, Cappello M (2007) Echinostome infection in Green frogs (Rana clamitans) is stage and age dependent. J Zool 271:455–462. https://doi.org/10.1111/j.1469-7998.2006.00229.x

    Article  Google Scholar 

  61. Hernández-Gómez O, Hoverman JT, Williams RN (2017) Cutaneous microbial community variation across populations of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis). Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.01379

  62. Hernández-Gómez O, Kimble SJA, Briggler JT, Williams RN (2017) Characterization of the cutaneous bacterial communities of two Giant salamander subspecies. Microb Ecol 73:445–454. https://doi.org/10.1007/s00248-016-0859-9

    Article  PubMed  Google Scholar 

  63. Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface Bacteria. Proc Natl Acad Sci U S A 105:17994–17999. https://doi.org/10.1073/pnas.0807920105

    Article  PubMed  PubMed Central  Google Scholar 

  64. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD (2012) PANDAseq: PAired-eND assembler for Illumina sequences. BMC Bioinformatics 13:31. https://doi.org/10.1186/1471-2105-13-31

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A, Clemente JC, Gilbert JA, Huse SM, Zhou H-W, Knight R, Caporaso JG (2014) Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. Peerj 2. https://doi.org/10.7717/peerj.545

    Article  Google Scholar 

  68. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. https://doi.org/10.1128/aem.03006-05

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642

    Article  CAS  Google Scholar 

  70. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–U11. https://doi.org/10.1038/nmeth.2276

    Article  PubMed  CAS  Google Scholar 

  71. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package

  72. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  Google Scholar 

  73. Chen J (2012) GUniFrac: generalized UniFrac distances

  74. Venebles WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York

    Book  Google Scholar 

  75. De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574

    Article  Google Scholar 

  76. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  77. Gao PP, Mao DQ, Luo Y, Wang LM, Xu BJ, Xu L (2012) Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res 46:2355–2364. https://doi.org/10.1016/j.watres.2012.02.004

    Article  PubMed  CAS  Google Scholar 

  78. Bernier SP, Surette MG (2013) Concentration-dependent activity of antibiotics in natural environments. Front Microbiol 4. https://doi.org/10.3389/fmicb.2013.00020

  79. Ding GC, Radl V, Schloter-Hai B, Jechalke S, Heuer H, Smalla K, Schloter M (2014) Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS One 9. https://doi.org/10.1371/journal.pone.0092958

    Article  CAS  Google Scholar 

  80. Islas-Espinoza M, Reid BJ, Wexler M, Bond PL (2012) Soil bacterial consortia and previous exposure enhance the biodegradation of sulfonamides from pig manure. Microb Ecol 64:140–151. https://doi.org/10.1007/s00248-012-0010-5

    Article  PubMed  CAS  Google Scholar 

  81. Jani AJ, Knapp RA, Briggs CJ (2017) Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proc R Soc B 284:20170944. https://doi.org/10.1098/rspb.2017.0944

    Article  PubMed  Google Scholar 

  82. Stutz WE, Blaustein AR, Briggs CJ, Hoverman JT, Rohr JR, Johnson PTJ (2017) Using multi-response models to investigate pathogen coinfections across scales: insights from emerging diseases of amphibians. Methods Ecol Evol 9:1109–1120. https://doi.org/10.1111/2041-210X.12938

    Article  PubMed  PubMed Central  Google Scholar 

  83. Carlson JM, Hyde ER, Petrosino JF, Manage ABW, Primm TP (2015) The host effects of Gambusia affinis with an antibiotic-disrupted microbiome. Comp Biochem Physiol C 178:163–168. https://doi.org/10.1016/j.cbpc.2015.10.004

    Article  CAS  Google Scholar 

  84. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/aem.71.12.8228-8235.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Belkaid Y, Segre JA (2014) Dialogue between skin microbiota and immunity. Science 346:954–959. https://doi.org/10.1126/science.1260144

    Article  PubMed  CAS  Google Scholar 

  86. Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc Natl Acad Sci U S A 99:9900–9904. https://doi.org/10.1073/pnas.152098899

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Galley JD, Bailey MT (2014) Impact of stressor exposure on the interplay between commensal microbiota and host inflammation. Gut Microbes 5:390–396. https://doi.org/10.4161/gmic.28683

    Article  PubMed  PubMed Central  Google Scholar 

  88. Simmaco M, Mignogna G, Barra D (1998) Antimicrobial peptides from amphibian skin: what do they tell us? Biopolymers 47:435–450. https://doi.org/10.1002/(sici)1097-0282(1998)47:6<435::aid-bip3>3.0.co;2-8

    Article  PubMed  CAS  Google Scholar 

  89. Simmaco M, Boman A, Mangoni ML, Mignogna G, Miele R, Barra D, Boman HG (1997) Effect of glucocorticoids on the synthesis of antimicrobial peptides in amphibian skin. FEBS Lett 416:273–275. https://doi.org/10.1016/s0014-5793(97)01216-7

    Article  PubMed  CAS  Google Scholar 

  90. Gomez D, Sunyer JO, Salinas I (2013) The mucosal immune system of Fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immunol 35:1729–1739. https://doi.org/10.1016/j.fsi.2013.09.032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Woodhams DC, Brandt H, Baumgartner S, Kielgast J, Kuepfer E (2014) Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLoS One 9:e96375. https://doi.org/10.1371/journal.pone.0104590

  92. Olson ME, Gard S, Brown M, Hampton R, Morck DW (1992) Flavobacterium-indologenes infection in leopard frogs. J Am Vet Med Assoc 201:1766–1770

    PubMed  CAS  Google Scholar 

  93. Lauer A, Simon MA, Banning JL, Andre E, Duncan K, Harris RN (2007) Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 630–640. https://doi.org/10.1643/0045-8511(2007)2007[630:ccbfte]2.0.co;2

    Article  Google Scholar 

  94. Mauel MJ, Miller DL, Frazier KS, Hines ME (2002) Bacterial pathogens isolated from cultured bullfrogs (Rana castesbeiana). J Vet Diagn Investig 14:431–433. https://doi.org/10.1177/104063870201400515

    Article  Google Scholar 

  95. Knutie SA, Wilkinson CL, Kohl KD, Rohr JR (2017) Early-life disruption of amphibian microbiota decreases later-life resistance to parasites. Nat Commun 8:86. https://doi.org/10.1038/s41467-017-00119-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

We thank the Purdue University Department of Forestry and Natural Resources Genetics Laboratory for allowing us to perform the microbiota laboratory work in their facility. We also thank the staff of the Cornell University Biotechnology Resource Center for their assistance in sequencing. Finally, we thank Nicholas Buss for collecting the leopard frog egg masses. All animals were handled in accordance with the Binghamton University IACUC protocol 757-16.

Funding

Funding for this research was provided by NSF DEB 1655190 to JH, NSF PRFB 1708926 to OHG, and by Binghamton University’s Sustainable Communities Transdisciplinary Areas of Excellence to VW.

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Author notes

  1. Obed Hernández-Gómez and Vanessa Wuerthner contributed equally to this work.

Authors and Affiliations

  1. Department of Environmental Science, Policy, and Management, University of California-Berkeley, Berkeley, CA, 94720, USA

    Obed Hernández-Gómez

  2. Biological Sciences Department, Binghamton University, Binghamton, NY, 13902, USA

    Vanessa Wuerthner & Jessica Hua

Authors
  1. Obed Hernández-Gómez
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  2. Vanessa Wuerthner
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  3. Jessica Hua
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Corresponding author

Correspondence to Obed Hernández-Gómez.

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The authors declare that they have no conflicts of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Hernández-Gómez, O., Wuerthner, V. & Hua, J. Amphibian Host and Skin Microbiota Response to a Common Agricultural Antimicrobial and Internal Parasite. Microb Ecol 79, 175–191 (2020). https://doi.org/10.1007/s00248-019-01351-5

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  • DOI: https://doi.org/10.1007/s00248-019-01351-5

Keywords

  • Lithobates pipiens
  • Sulfadimethoxine
  • Echinostomes
  • 16S rRNA