1887

Abstract

Amphibians have declined around the world in recent years, in parallel with the emergence of an epidermal disease called chytridiomycosis, caused by the chytrid fungus (). This disease has been associated with mass mortality in amphibians worldwide, including in Costa Rica, and is considered an important contributor to the disappearance of this group of vertebrates. While many species are susceptible to the disease, others show tolerance and manage to survive infection with the pathogen. We evaluated the pathogen circulating in Costa Rica and the capacity of amphibian skin bacteria to inhibit the growth of the pathogen . We isolated and characterized – genetically and morphologically – several isolates from areas with declining populations of amphibians. We determined that the circulating chytrid fungus in Costa Rica belongs to the virulent strain -GPL-2, which has been related to massive amphibian deaths worldwide; however, the isolates obtained showed genetic and morphological variation. Furthermore, we isolated epidermal bacteria from 12 amphibian species of surviving populations, some in danger of extinction, and evaluated their inhibitory activity against the collection of chytrid isolates. Through bioassays we confirmed the presence of chytrid-inhibitory bacterial genera in Costa Rican amphibians. However, we observed that the inhibition varied between different isolates of the same bacterial genus, and each bacterial isolation inhibited fungal isolation differently. In total, 14 bacterial isolates belonging to the genera , , , and showed inhibitory activity against all isolates. Given the observed variation both in the pathogen and in the bacterial inhibition capacity, it is highly relevant to include local isolates and to consider the origin of the microorganisms when performing infection tests aimed at developing and implementing mitigation strategies for chytridiomycosis.

Funding
This study was supported by the:
  • Ministerio de Ciencia Tecnología y Telecomunicaciones (CR) (Award 849-PINN-2015-I)
    • Principle Award Recipient: JuanG. Abarca
  • Universidad de Costa Rica (Award 810-B7-A46)
    • Principle Award Recipient: AdrianA Pinto-Tomás
  • Universidad de Costa Rica (Award 801-B2-029)
    • Principle Award Recipient: AdrianA Pinto-Tomás
  • U.S. Fish and Wildlife Service (Award 46-6003541)
    • Principle Award Recipient: StevenM. Whitfield
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2021-02-02
2021-10-17
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References

  1. IUCN The IUCN red list of threatened species. version 2019-2. https://www.iucnredlist.org ; 2020
  2. James TY, Litvintseva AP, Vilgalys R, Morgan JAT, Taylor JW et al. Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog 2009; 5:e1000458 [View Article][PubMed]
    [Google Scholar]
  3. Savage JM. The Amphibians and Reptiles of Costa Rica: a Herpetofauna Between Two Continents, Between Two Seas Chicago: University of Chicago Press; 2002 p 934 p
    [Google Scholar]
  4. Stuart SN, Chanson JS, Young BE, Rodrigues ASL et al. Status and trends of amphibian declines and extinctions worldwide. Science 2004; 306:1783–1786 [View Article][PubMed]
    [Google Scholar]
  5. Lips KR, Reeve JD, Witters LR. Ecological traits predicting amphibian population declines in Central America. Conserv Biol 2003; 17:1078–1088
    [Google Scholar]
  6. Pounds AJ, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 2006; 439:28–36
    [Google Scholar]
  7. Van Rooij P, Martel A, Haesebrouck F, Pasmans F. Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Vet Res 2015; 46:1–22
    [Google Scholar]
  8. Gascon C, Collins JP, Moore RD, Church DR, McKay JE. Amphibian conservation action plan. Gland, IUCN/SSC Amphibian Specialist Group. https://www.amphibianark.org/pdf/ACAP.pdf ; 2007
  9. Morens DM, Folkers GK, Fauci AS. What is a pandemic?. J Infect Dis 2009; 200:1018–1021
    [Google Scholar]
  10. Lambert MR, Womack MC, Byrne AQ, Hernández-Gómez O, Noss CF et al. Comment on “Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity”. Science 2020; 367:
    [Google Scholar]
  11. Berger L, Speare R, Daszak P, Green DE, Cunningham AA. Chytridiomycosis causes amphibian mortality associated with population declines in the rainforests of Australia and Central America. PNAS 1998; 95:9031–9036
    [Google Scholar]
  12. Fong JJ, Cheng TL, Bataille A, Pessier AP, Waldman B et al. Early 1900s detection of Batrachochytrium dendrobatidis in korean amphibians. PLoS ONE 2015; 10:e0115656
    [Google Scholar]
  13. Talley BL, Muletz CR, Vredenburg VT, Fleischer RC, Lips KR. A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888–1989). Biol Conserv 2015; 182:254–261
    [Google Scholar]
  14. Alvarado G. Batrachochytrium Dendrobatidis En Anuros De La Cordillera de Talamanca: Estudio Estructural, Molecular y Ecológico Master’s Thesis San José (CR): Universidad de Costa Rica; 2012 p 102
    [Google Scholar]
  15. Puschendorf R, Carnaval AC, Van Der Wal J, Zumbado Ulate H, Chaves G et al. Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool. Divers. Distrib 2009; 15:401–408
    [Google Scholar]
  16. Zumbado-Ulate H, Nelson KN, García-Rodríguez A, Chaves G, Arias E et al. Endemic infection of Batrachochytrium dendrobatidis in Costa Rica: implications for amphibian conservation at regional and species level. Diversity 2019; 11:129 [View Article]
    [Google Scholar]
  17. De León ME, Zumbado Ulate H, García Rodríguez A, Alvarado G, Sulaeman H et al. Batrachochytrium dendrobatidis infection in amphibians predates first known epizootic in Costa Rica. PLoS One 2019; 14:e0208969
    [Google Scholar]
  18. Bataille A, Fong JJ, Cha M, Wogan GOU, Baek HJ. Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Mol Ecol 2013; 22:4196–4209
    [Google Scholar]
  19. Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. PNAS 2011; 108:18732–18736
    [Google Scholar]
  20. Goka K, Yokoyama J, Une Y, Kuroki T, Suzuki K et al. Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Mol Ecol 2009; 18:4757–4774
    [Google Scholar]
  21. James TY, Toledo LP, Rodder D, Leite DS, Belasen AM et al. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecol Evol 2015; 5:4079–4097
    [Google Scholar]
  22. Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Viera CA et al. Novel, panzootic, and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Mol Ecol 2012; 21:5162–5177
    [Google Scholar]
  23. O’Hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 2018; 360:621–627
    [Google Scholar]
  24. Fisher MC, Bosch J, Yin Z, Stead DA, Walker J et al. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Mol Ecol 2009; 18:415–429
    [Google Scholar]
  25. Lambertini C, Becker CG, Jenkinson TS, Rodríguez D, Leite DS. Local phenotypic variation in amphibian-killing fungus predicts infection dynamics. Fungal Ecol 2016; 20:15–21
    [Google Scholar]
  26. Garner T, Garcia G, Carroll B, Fisher M. Using itraconazole to clear Batrachochytrium dendrobatidis infection, and subsequent depigmentation of Alytes muletensis tadpoles. Dis Aquat Organ 2009; 83:257–260
    [Google Scholar]
  27. Smith RK, Meredith H, Sutherland WJ. What works in conservation. Amphibian Conservation Cambridge, UK: Open Book Publishers; 2017 pp 9–65
    [Google Scholar]
  28. Bosch J, Sanchez Tome E, Fernandez Loras A, Oliver JA, Fisher MC et al. Successful elimination of a lethal wildlife infectious disease in nature. Biol Lett 2015; 11:20150874
    [Google Scholar]
  29. Woodhams DC, Bosch J, Briggs CJ, Cashins S, Davis LR et al. Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front Zool 2011; 8:1–23
    [Google Scholar]
  30. McCaffery R, Richards Zawacki CL, Lips KR. The demography of Atelopus decline: harlequin frog survival and abundance in central Panama prior to and during a disease outbreak. Glob Ecol Conserv 2015; 4:232–242
    [Google Scholar]
  31. Abarca JG, Chaves G, García Rodríguez A, Vargas R. Reconsidering extinction: rediscovery of Incilius holdridgei (Anura: Bufonidae) in Costa Rica after 25 years. Herpetol Rev 2010; 2010:150–152
    [Google Scholar]
  32. Puschendorf R, Bolaños F, Chaves G. The amphibian chytrid fungus along an altitudinal transect before the first reported declines in Costa Rica. Biol Conserv 2006; 132:136–142
    [Google Scholar]
  33. García Rodríguez A, Chaves G, Benavides Varela B, Puschendorf R. Where are the survivors? tracking relictual populations of endangered frogs in Costa Rica. Divers Distrib 2012; 18:204–212
    [Google Scholar]
  34. González-Maya JF, Belant JL, Wyatt SA, Schipper J, Cardenal J et al. Renewing hope: the rediscovery of Atelopus varius in Costa Rica. Amphibia-Reptilia 2013; 34:573–578 [View Article]
    [Google Scholar]
  35. Biton R, Geffen E, Vences M, Cohen O, Bailon S. The rediscovered Hula painted frog is a living fossil. Nat Commun 2013; 2013:1959
    [Google Scholar]
  36. Wickramasinghe LJM, Vidanapathirana DR, Airyarathne S, Rajeev G, Chanaka A et al. Lost and found: One of the world’s most elusive amphibians, Pseudophilautus stellatus (Kelaart 1853) rediscovered. Zootaxa 2013; 3620:112–128
    [Google Scholar]
  37. Chávez G, Zumbado-Ulate H, García-Rodríguez A, Gómez E, Vredenburg VT et al. Rediscovery of the critically endangered streamside frog, Craugastor taurus (Craugastoridae), in Costa Rica. Trop Conserv Sci 2014; 7:628–638 [View Article]
    [Google Scholar]
  38. Jiménez R, Alvarado G. Craugastor escoces (Anura: Craugastoridae) reappears after 30 years: rediscovery of an “extinct” Neotropical frog. Amphibia-Reptilia 2017; 38:1–3
    [Google Scholar]
  39. Tapia EE, Coloma LA, Pazmiño Otamendi G, Peñafiel N. Rediscovery of the nearly extinct longnose harlequin frog Atelopus longirostris (Bufonidae) in Junín, Imbabura, Ecuador. Neotrop Biodivers 2017; 3:157–167
    [Google Scholar]
  40. Berger L, Hyatt A, Speare R, Longcore JE. Lifecycle stages of Batrachochytrium dendrobatidis the amphibian chytrid. Dis Aquat Organ 2005; 68:51–63
    [Google Scholar]
  41. Rollins Smith LA, Conlon JM. Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev. Comp Immunol 2005; 29:589–598
    [Google Scholar]
  42. Woodhams DC, Ardipradja K, Alford RA, Marantelli G, Reinert LK et al. Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim Conserv 2007; 10:409–417
    [Google Scholar]
  43. Richmond JQ, Savage AE, Zamudio KR, Rosenblum EB. Toward immunogenetic studies of amphibian chytridiomycosis: linking innate and acquired immunity. BioScience 2009; 59:311–320
    [Google Scholar]
  44. Rosenblum EB, Poorten TJ, Joneson S, Settles M. Substrate-specific gene expression in Batrachochytrium dendrobatidis, the chytrid pathogen of amphibians. Plos One 2012; 7:2–10
    [Google Scholar]
  45. Savage AE, Zamudio KR. Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proc R Soc B 2016; 283:20153115
    [Google Scholar]
  46. Daskin JH, Alford RA, Puschendorf R. Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis . PLoS ONE 2011; 6:e26215
    [Google Scholar]
  47. McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM et al. Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 2014; 511:224–227
    [Google Scholar]
  48. Richards-Zawacki CL. Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proceedings of the Royal Society B: Biological Sciences 2010; 277:519–528 [View Article]
    [Google Scholar]
  49. McKenzie VJ, Bowers RM, Fierer N, Knight R, Lauber CL. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. Isme J 2012; 6:588–596
    [Google Scholar]
  50. Harris RN, James TY, Lauer A, Simon MA, Patel A. Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 2006; 3:53–56
    [Google Scholar]
  51. Woodhams DC, Vredenburg VT, Simon MA, Billheimer D, Shakhtour B et al. Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa . Biol Conserv 2007; 138:390–398 [View Article]
    [Google Scholar]
  52. Becker MH, Brucke RM, Schwantes CR, Harris RN, Minbiole KP. The bacterially produced metabolite violacein is associated with survival of amphibians infected with lethal fungus. Appl Environ Microbiol 2009; 209:6635–6638
    [Google Scholar]
  53. Loudon AH, Woodhams DC, Wegener L, Archer H, Knight R et al. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). Isme J 2014; 8:830–840
    [Google Scholar]
  54. Becker MH, Walke JB, Cikanek S, Savage AE, Mattheus N. Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus. Proc R Soc B 2016; 282:20142881
    [Google Scholar]
  55. Rebollar EA, Bridges T, Hughey MC, Medina D, Belden LK et al. Integrating the role of antifungal bacteria into skin symbiotic communities of three Neotropical frog species. The ISME Journal 2019; 13:1763–1775
    [Google Scholar]
  56. McDermott A. Fighting a fungal scourge. PNAS 2019; 116:20245–20249
    [Google Scholar]
  57. Kueneman JG, Woodhams DC, Harris R, Archer HM, Knight R et al. Probiotic treatment restores protection against lethal fungal infection lost during amphibian captivity. Proc. R. Soc. B 2016; 283:20161553
    [Google Scholar]
  58. Woodhams DC, Rollins-Smith LA, Reinert LK, Lam BA, Harris RN et al. Probiotics modulate a novel amphibian skin defense peptide that is antifungal and facilitates growth of antifungal bacteria. Microb Ecol 2020; 79:192–202 [View Article]
    [Google Scholar]
  59. Becker MH, Harris RN, Minbiole KPC, Schwantes CR, Rollins-Smith LA et al. Towards a better understanding of the use of probiotics for preventing chytridiomycosis in Panamanian golden frogs. EcoHealth 2011; 8:501–506
    [Google Scholar]
  60. Harrison XA, Sewell T, Fisher M, Antwis RE. Designing probiotic therapies with broad-spectrum activity against a wildlife pathogen. Front. Microbiol 2020; 10:3134
    [Google Scholar]
  61. Rebollar EA, Antwis RE, Becker MH, Belden LK, Bletz MC et al. Using “omics” and integrated multi-omics approaches to guide probiotic selection to mitigate chytridiomycosis and other emerging infectious diseases. Front Microbiol 2016; 7:
    [Google Scholar]
  62. Walke JB, Belden LK. Harnessing the microbiome to prevent fungal infections: lessons from amphibians. PLoS Pathog 2016; 12:e1005796
    [Google Scholar]
  63. Woodhams DC, Brandt H, Baumgartner S, Kielgast J, Kupfer E. Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLoS One 2014; 9:e96375 [View Article]
    [Google Scholar]
  64. Bletz MC, Loudon AH, Becker MH, Bell SC, Woodhams DC et al. Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecol Lett 2013; 16:807–820
    [Google Scholar]
  65. Whitfield SM, Alvarado G, Abarca J, Zumbado H, Zuñiga I et al. Differential patterns of Batrachochytrium dendrobatidis infection in relict amphibian populations following severe disease-associated declines. Dis Aquat Organ 2017; 126:33–41
    [Google Scholar]
  66. Whitfield SM, Lips KR, Donnelly MA. Amphibian decline and conservation in Central America. Copeia 2016; 104:351–379
    [Google Scholar]
  67. Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, Foster MS. (editors) Medición Y Monitoreo De La Diversidad Biológica. Métodos Estandarizados Para Anfibios Argentina: Smithsonian Institution; 2001
    [Google Scholar]
  68. Longcore JE, Pessier AP, Nichols DK. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 1999; 91:219–227 [View Article]
    [Google Scholar]
  69. Longcore JE. Culture techniques for amphibians chytrids. Paper Presented at: Amphibians Disease Conference/Workshop Australia: Cairns; 2000
    [Google Scholar]
  70. Boyle DG, Hyatt AD, Daszak P, Berger L, Longcore JE et al. Cryo-archiving of Batrachochytrium dendrobatidis and other chytriomycetes. Dis Aquat Organ 2003; 2003:59–64
    [Google Scholar]
  71. Flechas SV, Medina EM, Crawford AJ, Sarmiento C, Cárdenas ME et al. Characterization of the first Batrachochytrium dendrobatidis isolate from the Colombian Andes, an amphibian biodiversity hotspot. Eco Health 2013; 10:72–76
    [Google Scholar]
  72. Zhang YJ, Zhang S, Liu XZ, Wen HA, Wang M. A simple method of genomic DNA extraction suitable for analysis of bulk fungal strains. Lett Appl Microbiol 2010; 51:114–118
    [Google Scholar]
  73. Jenkinson TS, Betancourt CM, Lambertini C, Valencia Aguilar A, Rodríguez D et al. Amphibian-killing chytrid in Brazil comprises both locally endemic and globally expanding populations. Mol Ecol 2016; 25:2978–2996
    [Google Scholar]
  74. Swofford DL. PAUP. Version 4.0 b10. Phylogenetic Analysis Using Parsimony (and Other Methods). 2002, Sinauer, Sunderland.
  75. Reasoner DJ, Geldreich EE. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 1985; 49:1–7
    [Google Scholar]
  76. Barka EA, Vasta P, Sánchez L, Gavea Vaillant N, Jacquard C. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol R 2016; 80:1–43
    [Google Scholar]
  77. Hsu SC, Lockwood JL. Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 1975; 29:422–426 [View Article][PubMed]
    [Google Scholar]
  78. Wadetwar RN, Patil AT. Isolation and characterization of bioactive actinomycetes from soil in and around Nagpur. Int J Pharm Sci 2013; 4:1428–1433
    [Google Scholar]
  79. Zuñiga I. Evaluación De La Diversidad Bacteriana En La Piel De Los Anfibios De Costa Rica Y Su Potencial Actividad Antifúngica En Contra Del Hongo Patógeno Batrachochytrium Dendrobatidis.[bachelor’s Thesis] San José (CR: Universidad de Costa Rica; 2013 p 30
    [Google Scholar]
  80. Bell SC, Alford RA, Garland S, Padilla G, Thomas AD. Screening bacterial metabolites for inhibitory effects against Batrachochytrium dendrobatidis using a spectrophotometric assay. Dis Aquat Organ 2013; 103:77–85
    [Google Scholar]
  81. Chun J, Goodfellow M. A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int J Syst Bacteriol 1995; 45:240–245
    [Google Scholar]
  82. Altschul EF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410
    [Google Scholar]
  83. Byrne AQ, Vredenburg VT, Martel A, Pasmans F, Belle RC et al. Cryptic diversity of a widespread global pathogen reveals expanded threats to amphibian conservation. PNAS 2019; 116:20382–20387
    [Google Scholar]
  84. Lips KR, Diffendorf J, Mendelson JR, Sears MW. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. Plos Biol 2008; 6:441–454
    [Google Scholar]
  85. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA et al. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. PNAS 2006; 103:3165–3170
    [Google Scholar]
  86. Phillips BL, Puschendorf R. Do pathogens become more virulent as they spread? Evidence from the amphibian declines in Central America. Proc R Soc B 2013; 280:1290
    [Google Scholar]
  87. Voyles J. Phenotypic profiling of Batrachochytrium dendrobatidis, a lethal fungal pathogen of amphibians. Fungal Ecol 2011; 4:196–200
    [Google Scholar]
  88. Greenspan SE, Lambertini C, Carvalho T, James TY, Toledo LF et al. Hybrids of amphibian chytrid show high virulence in native hosts. Scientific reports 2018; 8:9600
    [Google Scholar]
  89. Voyles J, Woodhams DC, Saenz V, Byrne AQ, Perez R et al. Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science 2018; 359:1517–1519
    [Google Scholar]
  90. Flechas SV, Sarmiento C, Cárdenas ME, Medina EM, Restrepo S et al. Surviving chytridiomycosis: differential anti-Batrachochytrium dendrobatidis activity in bacterial isolates from three lowland species of Atelopus. Plos One 2012; 7:e44832
    [Google Scholar]
  91. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. Isme J 2009; 17:
    [Google Scholar]
  92. Lam BA, Walke JB, Vredenburg VT, Harris RN. Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa . Biol Conserv 2010; 143:529–531
    [Google Scholar]
  93. Lauer A, Simon MA, Banning JL, Andre E, Duncan K et al. Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007; 3:630–640
    [Google Scholar]
  94. Lauer A, Simon MA, Banning JL, Lam BA, Harris RN. Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. Isme J 2008; 2:145–157
    [Google Scholar]
  95. Walke JB, Harris RN, Reinert LK, Rollins Smith LA, Woodhams DC. Social immunity in amphibians: evidence for vertical transmission of innate defenses. Biotropica 2011; 43:396–400
    [Google Scholar]
  96. Walke JB, Becker MH, Hughey MH, Swartwout MC, Jensen RV et al. Dominance-function relationships in the amphibian skin microbiome. Environ Microbiol 2017; 19:3387–3397
    [Google Scholar]
  97. Antwis RE, Harrison X. Probiotic consortia are not uniformly effective against different amphibian chytrid pathogen isolates. Mol Ecol 2018; 27:577–589
    [Google Scholar]
  98. Antwis RE, Preziosi RF, Harrison XA, Garner TWJ. Amphibian symbiotic bacteria do not show a universal ability to inhibit growth of the global panzootic lineage of Batrachochytrium dendrobatidis . Appl. Environ Microbiol 2015; 81:3706–3711
    [Google Scholar]
  99. Bletz MC, Myers J, Woodhams DC, Rabemananjara FCE, Rakotonirina A et al. Estimating herd immunity to amphibian chytridiomycosis in Madagascar based on the defensive function of amphibian skin bacteria. Front Microbiol 1751; 2017:8
    [Google Scholar]
  100. Madison JD, Berg EA, Abarca JG, Whitfield SM, Gorbatenko O et al. Characterization of Batrachochytrium dendrobatidis inhibiting bacteria from amphibian populations in Costa Rica. Front Microbiol 2017; 290:
    [Google Scholar]
  101. Woodhams DC, Labumbard BC, Barnhart KL, Becker MH, Bletz MC et al. Prodigiosin, violacein, and volatile organic compounds produced by widespread cutaneous bacteria of amphibians can inhibit two Batrachochytrium fungal pathogens. Microb Ecol 2018
    [Google Scholar]
  102. Medina D, Walke JB, Gajewski Z, Becker MH, Swartwout MC et al. Culture media and individual hosts affect the recovery of culturable bacterial diversity from amphibian skin. Front Microbiol 2017; 8:1574
    [Google Scholar]
  103. Bell SC, Garland S, Alford RA. Increased numbers of culturable inhibitory bacterial taxa may mitigate the effects of Batrachochytrium dendrobatidis in australian wet tropics frogs. Front Microbiol 2018; 9:1604
    [Google Scholar]
  104. Berdy J. Bioactive microbial metabolites. J Antibiot 2005; 58:293–319
    [Google Scholar]
  105. Nett M, Ikeda H, Moore BS. Genomics basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 2009; 26:1362–1384
    [Google Scholar]
  106. Aggarwal N, Thind S, Sharma S. Role of secondary metabolites of actinomicetes in crop protection. In Subramaniam G, Arumugan S, Rajendran V. (editors) Plant Growth Promoting Actinobacteria Singapore: Springer; 2016 pp 99–121
    [Google Scholar]
  107. Byrne AQ, Rothstein AP, Poorten TJ, Erens J, Settles ML et al. Unlocking the story in the swab: A new genotyping assay for the amphibian chytrid fungus Batrachochytrium dendrobatidis . Mol Ecol Resour 2017; 17:1283–1292
    [Google Scholar]
  108. Fisher MC, Ghosh P, Shelton JMG, Bates K, Brookes L et al. Development and worldwide use of a non-lethal and minimal population-level impact protocols for the isolation of chytrids from amphibians. Sc Rep 2018; 8:7772
    [Google Scholar]
  109. Morgan JAT, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ et al. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis . Proc Natl Acad Sci U S A 2007; 104:13845–13850 [View Article][PubMed]
    [Google Scholar]
  110. James TY, Litvintseva AP, Vilgalys R, Morgan JAT, Taylor JW et al. Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog 2009; 5:e1000458 [View Article][PubMed]
    [Google Scholar]
  111. Morehouse EA, James TY, Ganley ARD, Vilgalys R, Berger L et al. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Mol Ecol 2003; 12:395–403 [View Article]
    [Google Scholar]
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