Skip to main content
Erschienen in: EcoHealth 1/2018

13.11.2017 | Original Contribution

Common Cutaneous Bacteria Isolated from Snakes Inhibit Growth of Ophidiomyces ophiodiicola

verfasst von: Aubree J. Hill, Jacob E. Leys, Danny Bryan, Fantasia M. Erdman, Katherine S. Malone, Gabrielle N. Russell, Roger D. Applegate, Heather Fenton, Kevin Niedringhaus, Andrew N. Miller, Matthew C. Allender, Donald M. Walker

Erschienen in: EcoHealth | Ausgabe 1/2018

Einloggen, um Zugang zu erhalten

Abstract

There is increasing concern regarding potential impacts of snake fungal disease (SFD), caused by Ophidiomyces ophiodiicola (Oo), on free-ranging snake populations in the eastern USA. The snake cutaneous microbiome likely serves as the first line of defense against Oo and other pathogens; however, little is known about microbial associations in snakes. The objective of this study was to better define the composition and immune function of the snake cutaneous microbiome. Eight timber rattlesnakes (Crotalus horridus) and four black racers (Coluber constrictor) were captured in Arkansas and Tennessee, with some snakes exhibiting signs of SFD. Oo was detected through real-time qPCR in five snakes. Additional histopathological techniques confirmed a diagnosis of SFD in one racer, the species’ first confirmed case of SFD in Tennessee. Fifty-eight bacterial and five fungal strains were isolated from skin swabs and identified with Sanger sequencing. Non-metric multidimensional scaling and PERMANOVA analyses indicated that the culturable microbiome does not differ between snake species. Fifteen bacterial strains isolated from rattlesnakes and a single strain isolated from a racer inhibited growth of Oo in vitro. Results shed light on the culturable cutaneous microbiome of snakes and probiotic members that may play a role in fighting an emergent disease.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Alford RA, Richards SJ. (1999) Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30: 133-165CrossRef Alford RA, Richards SJ. (1999) Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30: 133-165CrossRef
Zurück zum Zitat Allender MC, Dreslik M, Wylie S, Phillips C, Wylie DB, Maddox C. (2011) Chrysosporium sp. infection in Eastern massasauga rattlesnakes. Emerging Infectious Diseases 17(12): 2383-2385CrossRefPubMedPubMedCentral Allender MC, Dreslik M, Wylie S, Phillips C, Wylie DB, Maddox C. (2011) Chrysosporium sp. infection in Eastern massasauga rattlesnakes. Emerging Infectious Diseases 17(12): 2383-2385CrossRefPubMedPubMedCentral
Zurück zum Zitat Allender MC, Baker S, Wylie D, Loper D, Dreslik M, Phillips C, Maddox C, Driskell EA. (2015a) Development of snake fungal disease after experimental challenge with Ophidiomyces ophiodiicola in cottonmouths (Agkistrodon piscivorous). PLOS ONE 10(10): e0140193CrossRefPubMedPubMedCentral Allender MC, Baker S, Wylie D, Loper D, Dreslik M, Phillips C, Maddox C, Driskell EA. (2015a) Development of snake fungal disease after experimental challenge with Ophidiomyces ophiodiicola in cottonmouths (Agkistrodon piscivorous). PLOS ONE 10(10): e0140193CrossRefPubMedPubMedCentral
Zurück zum Zitat Allender MC, Bunick D, Dzhaman E, Burrus L, Maddox C. (2015b) Development and use of a real-time polymerase chain reaction assay for the detection of Ophidiomyces ophiodiicola in snakes. Journal of Veterinary Diagnostic Investigation 27(2): 217-220CrossRefPubMed Allender MC, Bunick D, Dzhaman E, Burrus L, Maddox C. (2015b) Development and use of a real-time polymerase chain reaction assay for the detection of Ophidiomyces ophiodiicola in snakes. Journal of Veterinary Diagnostic Investigation 27(2): 217-220CrossRefPubMed
Zurück zum Zitat Allender MC, Raudabaugh DB, Gleason FH, Miller AN. (2015c) The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations. Fungal Ecology 17: 187-196CrossRef Allender MC, Raudabaugh DB, Gleason FH, Miller AN. (2015c) The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations. Fungal Ecology 17: 187-196CrossRef
Zurück zum Zitat Ayoubi N, Soleimani MJ. (2015) Strawberry fruit rot caused by Neopestalotiopsis iranensis sp. nov., and N. mesopotamica. Current Microbiology 10: 1-8 Ayoubi N, Soleimani MJ. (2015) Strawberry fruit rot caused by Neopestalotiopsis iranensis sp. nov., and N. mesopotamica. Current Microbiology 10: 1-8
Zurück zum Zitat Belden LK, Harris RN. (2007) Infectious diseases in wildlife: the community ecology context. Frontiers in Ecology and the Environment 5(10): 533-539CrossRef Belden LK, Harris RN. (2007) Infectious diseases in wildlife: the community ecology context. Frontiers in Ecology and the Environment 5(10): 533-539CrossRef
Zurück zum Zitat Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB. (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323(5911): 227CrossRefPubMed Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB. (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323(5911): 227CrossRefPubMed
Zurück zum Zitat Bletz MC, Loudon AH, Becker MH, Bell SC, Woodhams DC, Minbole KPC, Harris RN. (2013) Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecology Letters 16: 807-820CrossRefPubMed Bletz MC, Loudon AH, Becker MH, Bell SC, Woodhams DC, Minbole KPC, Harris RN. (2013) Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecology Letters 16: 807-820CrossRefPubMed
Zurück zum Zitat Bohuski E, Lorch JM, Griffin KM, Blehert DS. (2015) TaqMan real-time polymerase chain reaction for detection of Ophidiomyces ophiodiicola, the fungus associated with snake fungal disease. BioMed Central Veterinary Research 11(1): 1 Bohuski E, Lorch JM, Griffin KM, Blehert DS. (2015) TaqMan real-time polymerase chain reaction for detection of Ophidiomyces ophiodiicola, the fungus associated with snake fungal disease. BioMed Central Veterinary Research 11(1): 1
Zurück zum Zitat Bosch J, MartÍnez-Solano I, GarcÍa-Paris M. (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biological Conservation 97(3): 331-337CrossRef Bosch J, MartÍnez-Solano I, GarcÍa-Paris M. (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biological Conservation 97(3): 331-337CrossRef
Zurück zum Zitat Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature methods 7(5): 335-6.CrossRefPubMedPubMedCentral Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature methods 7(5): 335-6.CrossRefPubMedPubMedCentral
Zurück zum Zitat Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6(8): 1621-1624CrossRefPubMedPubMedCentral Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6(8): 1621-1624CrossRefPubMedPubMedCentral
Zurück zum Zitat Case TJ, Bolger DT. (1991) The role of introduced species in shaping the distribution and abundance of island reptiles. Evolutionary Ecology 5(3): 272-290CrossRef Case TJ, Bolger DT. (1991) The role of introduced species in shaping the distribution and abundance of island reptiles. Evolutionary Ecology 5(3): 272-290CrossRef
Zurück zum Zitat Cheatwood JL, Jacobson ER, May PG, Farrell TM, Homer BL, Samuelson DA, Kimbrough JW. (2003). An outbreak of fungal dermatitis and stomatitis in a free-ranging population of pigmy rattlesnakes (Sistrurus miliarius barbouri) in Florida. Journal of Wildlife Diseases 39(2): 329-337CrossRefPubMed Cheatwood JL, Jacobson ER, May PG, Farrell TM, Homer BL, Samuelson DA, Kimbrough JW. (2003). An outbreak of fungal dermatitis and stomatitis in a free-ranging population of pigmy rattlesnakes (Sistrurus miliarius barbouri) in Florida. Journal of Wildlife Diseases 39(2): 329-337CrossRefPubMed
Zurück zum Zitat Clark RW, Marchand MN, Clifford BJ, Stechert R, Stephens S. (2011) Decline of an isolated timber rattlesnake (Crotalus horridus) population: interactions between climate change, disease, and loss of genetic diversity. Biological Conservation 144(2): 886-891CrossRef Clark RW, Marchand MN, Clifford BJ, Stechert R, Stephens S. (2011) Decline of an isolated timber rattlesnake (Crotalus horridus) population: interactions between climate change, disease, and loss of genetic diversity. Biological Conservation 144(2): 886-891CrossRef
Zurück zum Zitat Cornelison CT, Keel MK, Gabriel KT, Barlament CK, Tucker TA, Pierce GE, Crow SA. (2014) A preliminary report on the contact-independent antagonism of Pseudogymnoascus destructans by Rhodococcus rhodochrous strain AP96253. BioMed Central Microbiology 14(1): 246PubMedPubMedCentral Cornelison CT, Keel MK, Gabriel KT, Barlament CK, Tucker TA, Pierce GE, Crow SA. (2014) A preliminary report on the contact-independent antagonism of Pseudogymnoascus destructans by Rhodococcus rhodochrous strain AP96253. BioMed Central Microbiology 14(1): 246PubMedPubMedCentral
Zurück zum Zitat Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R. (1999) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5(6): 735CrossRefPubMedPubMedCentral Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R. (1999) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5(6): 735CrossRefPubMedPubMedCentral
Zurück zum Zitat Daszak P, Cunningham AA, Hyatt AD. (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9(2): 141-150CrossRef Daszak P, Cunningham AA, Hyatt AD. (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9(2): 141-150CrossRef
Zurück zum Zitat Dipineto L, Russo TP, Calabria M, De Rosa L, Capasso M, Menna LF, Borrelli L, Fioretti A. Oral flora of Python regius kept as pets. (2014) Letters in Applied Microbiology 58(5):462-5.CrossRefPubMed Dipineto L, Russo TP, Calabria M, De Rosa L, Capasso M, Menna LF, Borrelli L, Fioretti A. Oral flora of Python regius kept as pets. (2014) Letters in Applied Microbiology 58(5):462-5.CrossRefPubMed
Zurück zum Zitat Dolinski AC, Allender MC, Hsiao V, Maddox CW. (2014) Systemic Ophidiomyces ophiodiicola infection in a free-ranging plains garter snake (Thamnophis radix). Journal of Herpetological Medicine and Surgery 24(1): 7-10CrossRef Dolinski AC, Allender MC, Hsiao V, Maddox CW. (2014) Systemic Ophidiomyces ophiodiicola infection in a free-ranging plains garter snake (Thamnophis radix). Journal of Herpetological Medicine and Surgery 24(1): 7-10CrossRef
Zurück zum Zitat Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484(7393): 186-194CrossRefPubMed Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484(7393): 186-194CrossRefPubMed
Zurück zum Zitat Gargas A, Trest M, Christensen M, Volk T, Blehert D. (2009) Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108(1): 147-154CrossRef Gargas A, Trest M, Christensen M, Volk T, Blehert D. (2009) Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108(1): 147-154CrossRef
Zurück zum Zitat Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fisher MC. (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2(3): 455-459CrossRefPubMedPubMedCentral Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fisher MC. (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2(3): 455-459CrossRefPubMedPubMedCentral
Zurück zum Zitat Gefrides LA, Powell MC, Donley MA, Kahn R. (2010) UV irradiation and autoclave treatment for elimination of contaminating DNA from laboratory consumables. Forensic Science Internationals: Genetics 4: 89-94CrossRef Gefrides LA, Powell MC, Donley MA, Kahn R. (2010) UV irradiation and autoclave treatment for elimination of contaminating DNA from laboratory consumables. Forensic Science Internationals: Genetics 4: 89-94CrossRef
Zurück zum Zitat Gil-Turnes MS, Fenical W. (1992) Embryos of Homarus americanus are protected by epibiotic bacteria. The Biological Bulletin 182: 105–108CrossRefPubMed Gil-Turnes MS, Fenical W. (1992) Embryos of Homarus americanus are protected by epibiotic bacteria. The Biological Bulletin 182: 105–108CrossRefPubMed
Zurück zum Zitat Glorioso BM, Waddle JH, Green DE, Lorch JM. (2016) First documented case of snake fungal disease in a free-ranging wild snake in Louisiana. Southeastern Naturalist 2016 Glorioso BM, Waddle JH, Green DE, Lorch JM. (2016) First documented case of snake fungal disease in a free-ranging wild snake in Louisiana. Southeastern Naturalist 2016
Zurück zum Zitat Guthrie AL, Knowles S, Ballmann AE, Lorch JM. (2015) Detection of snake fungal disease due to Ophidiomyces ophiodiicola in Virginia, USA. Journal of Wildlife Diseases 52(1): 143-149CrossRef Guthrie AL, Knowles S, Ballmann AE, Lorch JM. (2015) Detection of snake fungal disease due to Ophidiomyces ophiodiicola in Virginia, USA. Journal of Wildlife Diseases 52(1): 143-149CrossRef
Zurück zum Zitat Harris RN, James TY, Lauer A, Simon MA, Patel A. (2006) Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3: 53–56CrossRef Harris RN, James TY, Lauer A, Simon MA, Patel A. (2006) Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3: 53–56CrossRef
Zurück zum Zitat Harris RN, Lauer A, Simon MA, Banning JL, Alford RA. (2009) Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Diseases of Aquatic Organisms 83(1): 11–6CrossRefPubMed Harris RN, Lauer A, Simon MA, Banning JL, Alford RA. (2009) Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Diseases of Aquatic Organisms 83(1): 11–6CrossRefPubMed
Zurück zum Zitat Harris NB, Rogers DG. (2001) Septicemia associated with Stenotrophomonas maltophilia in a West African dwarf crocodile (Osteolaemus tetraspis subsp. tetraspis). Journal of Veterinary Diagnostic Investigation 13(3): 255-258CrossRefPubMed Harris NB, Rogers DG. (2001) Septicemia associated with Stenotrophomonas maltophilia in a West African dwarf crocodile (Osteolaemus tetraspis subsp. tetraspis). Journal of Veterinary Diagnostic Investigation 13(3): 255-258CrossRefPubMed
Zurück zum Zitat Hinton TG, Scott DE. (1990) Life history and ecology of the slider turtle. In: Radioecological Techniques for Herpetology, with an Emphasis on Freshwater Turtles. Washington, DC, USA: Smithsonian Institute Press, pp 267-287 Hinton TG, Scott DE. (1990) Life history and ecology of the slider turtle. In: Radioecological Techniques for Herpetology, with an Emphasis on Freshwater Turtles. Washington, DC, USA: Smithsonian Institute Press, pp 267-287
Zurück zum Zitat Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL. (2000) Quantitative evidence for global amphibian population declines. Nature 404(6779): 752-755CrossRefPubMed Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL. (2000) Quantitative evidence for global amphibian population declines. Nature 404(6779): 752-755CrossRefPubMed
Zurück zum Zitat Irianto A, Austin B. (2002) Probiotics in aquaculture. Journal of Fish Diseases 25: 633–642CrossRef Irianto A, Austin B. (2002) Probiotics in aquaculture. Journal of Fish Diseases 25: 633–642CrossRef
Zurück zum Zitat Jayawardena RS, Zhang W, Liu M, Maharachchikumbura SS, Zhou Y, Huang J, Nilthong S, Wang Z, Li X, Yan J, Hyde KD. (2015) Identification and characterization of Pestalotiopsis-like fungi related to grapevine diseases in China. Fungal Biology 119: 348-61CrossRefPubMed Jayawardena RS, Zhang W, Liu M, Maharachchikumbura SS, Zhou Y, Huang J, Nilthong S, Wang Z, Li X, Yan J, Hyde KD. (2015) Identification and characterization of Pestalotiopsis-like fungi related to grapevine diseases in China. Fungal Biology 119: 348-61CrossRefPubMed
Zurück zum Zitat Jho YS, Park DH, Lee JH, Cha SY, Han JS. (2011) Identification of bacteria from the oral cavity and cloaca of snakes imported from Vietnam. Laboratory Animal Research 27(3): 213-217CrossRefPubMedPubMedCentral Jho YS, Park DH, Lee JH, Cha SY, Han JS. (2011) Identification of bacteria from the oral cavity and cloaca of snakes imported from Vietnam. Laboratory Animal Research 27(3): 213-217CrossRefPubMedPubMedCentral
Zurück zum Zitat Junior F, Rui S, Siqueira AK, Campagner MV, Salerno T, Soares T, Lucheis SB, Paes AC, Barraviera B. (2009) Comparison of wildlife and captivity rattlesnakes (Crotalus durissus terrificus) microbiota. Pesquisa Veterinária Brasileira 2009(12): 999-1003.CrossRef Junior F, Rui S, Siqueira AK, Campagner MV, Salerno T, Soares T, Lucheis SB, Paes AC, Barraviera B. (2009) Comparison of wildlife and captivity rattlesnakes (Crotalus durissus terrificus) microbiota. Pesquisa Veterinária Brasileira 2009(12): 999-1003.CrossRef
Zurück zum Zitat Kado CI. (2006) Erwinia and related genera. In The Prokaryotes. New York: Springer, pp. 443–450 Kado CI. (2006) Erwinia and related genera. In The Prokaryotes. New York: Springer, pp. 443–450
Zurück zum Zitat Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiß M, Larsson, KH. (2013) Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22: 5271-5277CrossRefPubMed Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiß M, Larsson, KH. (2013) Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22: 5271-5277CrossRefPubMed
Zurück zum Zitat Last LA, Fenton H, Gonyor-McGuire J, Moore M, Yabsley MJ. (2016) Snake fungal disease caused by Ophidiomyces ophiodiicola in a free-ranging mud snake (Farancia abacura). Journal of Veterinary Diagnostic Investigation. 2016 Oct 3:1040638716663250. Last LA, Fenton H, Gonyor-McGuire J, Moore M, Yabsley MJ. (2016) Snake fungal disease caused by Ophidiomyces ophiodiicola in a free-ranging mud snake (Farancia abacura). Journal of Veterinary Diagnostic Investigation. 2016 Oct 3:1040638716663250.
Zurück zum Zitat 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 3: 630–640CrossRef 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 3: 630–640CrossRef
Zurück zum Zitat Lips KR. (1998) Decline of a tropical montane amphibian fauna. Conservation Biology 12.1: 106–17CrossRef Lips KR. (1998) Decline of a tropical montane amphibian fauna. Conservation Biology 12.1: 106–17CrossRef
Zurück zum Zitat Looney WJ, Narita M, Mühlemann K. (2009) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. The lancet: infectious diseases 9(5): 312–23CrossRef Looney WJ, Narita M, Mühlemann K. (2009) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. The lancet: infectious diseases 9(5): 312–23CrossRef
Zurück zum Zitat Lorch JM, Lankton J, Werner K, Falendysz EA, McCurley K, Blehert DS. (2015) Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. MBio 6(6): e01534-15CrossRefPubMedPubMedCentral Lorch JM, Lankton J, Werner K, Falendysz EA, McCurley K, Blehert DS. (2015) Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. MBio 6(6): e01534-15CrossRefPubMedPubMedCentral
Zurück zum Zitat Maraki S, Sarchianaki E, Barbagadakis S. (2012) Myroides odoratimimus soft tissue infection in an immunocompetent child following a pig bite: case report and literature review. The Brazilian Journal of Infectious Diseases 16(4): 390-2.CrossRefPubMed Maraki S, Sarchianaki E, Barbagadakis S. (2012) Myroides odoratimimus soft tissue infection in an immunocompetent child following a pig bite: case report and literature review. The Brazilian Journal of Infectious Diseases 16(4): 390-2.CrossRefPubMed
Zurück zum Zitat Martel A, Blooi M, Adriaensen C, Van Rooij P, Beukema W, Fisher MC, Farrer RA, Schmidt BR, Tobler U, Goka K, Lips KR. (2014) Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346(6209): 630-631CrossRefPubMedPubMedCentral Martel A, Blooi M, Adriaensen C, Van Rooij P, Beukema W, Fisher MC, Farrer RA, Schmidt BR, Tobler U, Goka K, Lips KR. (2014) Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346(6209): 630-631CrossRefPubMedPubMedCentral
Zurück zum Zitat McBride MP, Wojick KB, Georoff TA, Kimbro J, Garner MM, Wang X, Childress AL, Wellehan Jr., JF. (2015) Ophidiomyces ophiodiicola dermatitis in eight free-ranging timber rattlesnakes (Crotalus horridus) from Massachusetts. Journal of Zoo and Wildlife Medicine 46(1): 86-94CrossRefPubMed McBride MP, Wojick KB, Georoff TA, Kimbro J, Garner MM, Wang X, Childress AL, Wellehan Jr., JF. (2015) Ophidiomyces ophiodiicola dermatitis in eight free-ranging timber rattlesnakes (Crotalus horridus) from Massachusetts. Journal of Zoo and Wildlife Medicine 46(1): 86-94CrossRefPubMed
Zurück zum Zitat Miller D, Radi Z, Stiver S, Thornhill T. (2004) Cutaneous and pulmonary mycosis in green anacondas (Euncectes murinus). Journal of Zoo and Wildlife Medicine 35(4): 557-561CrossRefPubMed Miller D, Radi Z, Stiver S, Thornhill T. (2004) Cutaneous and pulmonary mycosis in green anacondas (Euncectes murinus). Journal of Zoo and Wildlife Medicine 35(4): 557-561CrossRefPubMed
Zurück zum Zitat Nichols D, Weyant R, Lamirande E, Sigler L, Mason R. (1999) Fatal mycotic dermatitis in captive brown tree snakes (Boiga irregularis). Journal of Zoo and Wildlife Medicine 30(1): 111-118PubMed Nichols D, Weyant R, Lamirande E, Sigler L, Mason R. (1999) Fatal mycotic dermatitis in captive brown tree snakes (Boiga irregularis). Journal of Zoo and Wildlife Medicine 30(1): 111-118PubMed
Zurück zum Zitat Paré JA, Sigler L. (2016) An overview of reptile fungal pathogens in the genera Nannizziopsis, Paranannizziopsis, and Ophidiomyces. Journal of Herpetological Medicine and Surgery 26(1-2): 46-53CrossRef Paré JA, Sigler L. (2016) An overview of reptile fungal pathogens in the genera Nannizziopsis, Paranannizziopsis, and Ophidiomyces. Journal of Herpetological Medicine and Surgery 26(1-2): 46-53CrossRef
Zurück zum Zitat Park ST, Collingwood AM, St-Hilaire S, Sheridan PP. (2014) Inhibition of Batrachochytrium dendrobatidis caused by bacteria isolated from the skin of boreal toads, Anaxyrus (Bufo) boreas, from Grand Teton National Park, Wyoming, USA. Microbiology Insights 7: 1CrossRefPubMedPubMedCentral Park ST, Collingwood AM, St-Hilaire S, Sheridan PP. (2014) Inhibition of Batrachochytrium dendrobatidis caused by bacteria isolated from the skin of boreal toads, Anaxyrus (Bufo) boreas, from Grand Teton National Park, Wyoming, USA. Microbiology Insights 7: 1CrossRefPubMedPubMedCentral
Zurück zum Zitat Pechmann JHK, Wilbur HM. (1994) Putting declining amphibian populations in perspective: natural fluctuations and human impacts. Herpetologica 1994: 65-84 Pechmann JHK, Wilbur HM. (1994) Putting declining amphibian populations in perspective: natural fluctuations and human impacts. Herpetologica 1994: 65-84
Zurück zum Zitat Perdomo H, Cano J, Gené J, García D, Hernández M, Guarro J. (2013) Polyphasic analysis of Purpureocillium lilacinum isolates from different origins and proposal of the new species Purpureocillium lavendulum. Mycologia 105(1): 151-161CrossRefPubMed Perdomo H, Cano J, Gené J, García D, Hernández M, Guarro J. (2013) Polyphasic analysis of Purpureocillium lilacinum isolates from different origins and proposal of the new species Purpureocillium lavendulum. Mycologia 105(1): 151-161CrossRefPubMed
Zurück zum Zitat Rajeev S, Sutton DA, Wickes BL, Miller DL, Giri D, Van Meter M, Thompson EH, Rinaldi MG, Romanelli AM, Cano JF, Guarro J. (2009) Isolation and characterization of a new fungal species, Chrysosporium ophiodiicola, from a mycotic granuloma of a black rat snake (Elaphe obsoleta obsoleta). Journal of Clinical Microbiology 47(4), 1264-1268CrossRefPubMed Rajeev S, Sutton DA, Wickes BL, Miller DL, Giri D, Van Meter M, Thompson EH, Rinaldi MG, Romanelli AM, Cano JF, Guarro J. (2009) Isolation and characterization of a new fungal species, Chrysosporium ophiodiicola, from a mycotic granuloma of a black rat snake (Elaphe obsoleta obsoleta). Journal of Clinical Microbiology 47(4), 1264-1268CrossRefPubMed
Zurück zum Zitat Reavill DR, Schmidt RE. (2012) Mycobacterial lesions in fish, amphibians, reptiles, rodents, lagomorphs, and ferrets with reference to animal models. Veterinary Clinics of North America - Exotic Animal Practice 15(1): 25CrossRefPubMed Reavill DR, Schmidt RE. (2012) Mycobacterial lesions in fish, amphibians, reptiles, rodents, lagomorphs, and ferrets with reference to animal models. Veterinary Clinics of North America - Exotic Animal Practice 15(1): 25CrossRefPubMed
Zurück zum Zitat Rödder D, Kielgast J, Bielby J, Schmidtlein S, Bosch J, Garner TW, Veith M, Walker S, Fisher MC, Lötters S. (2009) Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity 1(1): 52-66CrossRef Rödder D, Kielgast J, Bielby J, Schmidtlein S, Bosch J, Garner TW, Veith M, Walker S, Fisher MC, Lötters S. (2009) Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity 1(1): 52-66CrossRef
Zurück zum Zitat Schroff S, Schmidt V, Kiefer I, Krautwald-Junghanns ME, Pees M. (2010) Ultrasonographic diagnosis of an endocarditis valvularis in a Burmese python (Python molurus bivittatus) with pneumonia. Journal of Zoo and Wildlife Medicine 41(4): 721-4CrossRefPubMed Schroff S, Schmidt V, Kiefer I, Krautwald-Junghanns ME, Pees M. (2010) Ultrasonographic diagnosis of an endocarditis valvularis in a Burmese python (Python molurus bivittatus) with pneumonia. Journal of Zoo and Wildlife Medicine 41(4): 721-4CrossRefPubMed
Zurück zum Zitat Sheridan BS, Wilson GR, Weldon PJ. (1989) Aerobic bacteria from the skin of the rattlesnake, Crotalus atrox. Journal of Herpetology 23(2): 200-202CrossRef Sheridan BS, Wilson GR, Weldon PJ. (1989) Aerobic bacteria from the skin of the rattlesnake, Crotalus atrox. Journal of Herpetology 23(2): 200-202CrossRef
Zurück zum Zitat Short DP, O’Donnell K, Thrane U, Nielsen KF, Zhang N, Juba JH, Geiser DM. (2013) Phylogenetic relationships among members of the Fusarium solani species complex in human infections and the descriptions of F. keratoplasticum sp. nov. and F. petroliphilum stat. nov. Fungal Genetics and Biology 53: 59-70CrossRefPubMed Short DP, O’Donnell K, Thrane U, Nielsen KF, Zhang N, Juba JH, Geiser DM. (2013) Phylogenetic relationships among members of the Fusarium solani species complex in human infections and the descriptions of F. keratoplasticum sp. nov. and F. petroliphilum stat. nov. Fungal Genetics and Biology 53: 59-70CrossRefPubMed
Zurück zum Zitat Smeekens SP, Huttenhower C, Riza A, Van de Veerdonk FL, Zeeuwen PL, Schalkwijk J, Van der Meer JW, Xavier RJ, Netea MG, Gevers D. (2014) Skin microbiome imbalance in patients with STAT1/STAT3 defects impairs innate host defense responses. Journal of Innate Immunity 6(3): 253-262CrossRefPubMed Smeekens SP, Huttenhower C, Riza A, Van de Veerdonk FL, Zeeuwen PL, Schalkwijk J, Van der Meer JW, Xavier RJ, Netea MG, Gevers D. (2014) Skin microbiome imbalance in patients with STAT1/STAT3 defects impairs innate host defense responses. Journal of Innate Immunity 6(3): 253-262CrossRefPubMed
Zurück zum Zitat Smith KF, Sax DF, Lafferty KD. (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20(5): 1349-1357CrossRefPubMed Smith KF, Sax DF, Lafferty KD. (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20(5): 1349-1357CrossRefPubMed
Zurück zum Zitat Tetzlaff SJ, Allender M, Ravesi M, Smith J, Kingsbury B. (2015) First report of snake fungal disease from Michigan, USA, involving Massasaugas, Sistrurus catenatus (Rafinesque 1818). Herpetology Notes 8: 31-33 Tetzlaff SJ, Allender M, Ravesi M, Smith J, Kingsbury B. (2015) First report of snake fungal disease from Michigan, USA, involving Massasaugas, Sistrurus catenatus (Rafinesque 1818). Herpetology Notes 8: 31-33
Zurück zum Zitat Verschuere L, Rombaut G, Sorgeloos P, Verstraete W. (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews 64: 655–671CrossRefPubMedPubMedCentral Verschuere L, Rombaut G, Sorgeloos P, Verstraete W. (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews 64: 655–671CrossRefPubMedPubMedCentral
Zurück zum Zitat Walker DM, Castlebury LA, Rossman AY, Sogonov MV, White Jr. JF. (2010) Systematics of the genus Gnomoniopsis (Gnomoniaceae, Diaporthales) based on a three gene phylogeny, host associations, and morphology. Mycologia 102: 1479–1496CrossRefPubMed Walker DM, Castlebury LA, Rossman AY, Sogonov MV, White Jr. JF. (2010) Systematics of the genus Gnomoniopsis (Gnomoniaceae, Diaporthales) based on a three gene phylogeny, host associations, and morphology. Mycologia 102: 1479–1496CrossRefPubMed
Zurück zum Zitat Walker DM, Castlebury LA, Rossman AY, Mejía LC, White Jr. JF. (2012) Phylogeny and taxonomy of Ophiognomonia (Gnomoniaceae, Diaporthales), including twenty-five new species in this highly diverse genus. Fungal Diversity 57(1): 85-147CrossRef Walker DM, Castlebury LA, Rossman AY, Mejía LC, White Jr. JF. (2012) Phylogeny and taxonomy of Ophiognomonia (Gnomoniaceae, Diaporthales), including twenty-five new species in this highly diverse genus. Fungal Diversity 57(1): 85-147CrossRef
Zurück zum Zitat Walker DM, Lawrence BR, Esterline D, McAndrew M, Edelbrock J, Graham SP, Kelehear C. (2015) A novel protocol for removing environmental microbes from amphibian skin. Herpetological Reviews 46: 349–353 Walker DM, Lawrence BR, Esterline D, McAndrew M, Edelbrock J, Graham SP, Kelehear C. (2015) A novel protocol for removing environmental microbes from amphibian skin. Herpetological Reviews 46: 349–353
Zurück zum Zitat White TJ, Bruns T, Lee S, Taylor J. (1990) Amplification and direct sequencing of fungal ribosomal DNA for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. Innis MA, Gelfand DH, Sninsky JJ, White TJ (editors), San Diego, CA, USA: Academic Press, pp 315–322 White TJ, Bruns T, Lee S, Taylor J. (1990) Amplification and direct sequencing of fungal ribosomal DNA for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. Innis MA, Gelfand DH, Sninsky JJ, White TJ (editors), San Diego, CA, USA: Academic Press, pp 315–322
Zurück zum Zitat Woodhams DC, Alford R, Briggs C, Johnson M, Rollins-Smith L. (2008) Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology 89 (6): 1627-1639CrossRefPubMed Woodhams DC, Alford R, Briggs C, Johnson M, Rollins-Smith L. (2008) Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology 89 (6): 1627-1639CrossRefPubMed
Zurück zum Zitat Woodhams DC, Brandt H, Baumgartner S, Kielgast J, Küpfer E, Tobler U, Davis LR, Schmidt BR, Bel C, Hodel S, Knight R, McKenzie V. (2014) Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLOS ONE 9(4): e96375CrossRefPubMedPubMedCentral Woodhams DC, Brandt H, Baumgartner S, Kielgast J, Küpfer E, Tobler U, Davis LR, Schmidt BR, Bel C, Hodel S, Knight R, McKenzie V. (2014) Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLOS ONE 9(4): e96375CrossRefPubMedPubMedCentral
Zurück zum Zitat Woodhams DC, Bletz M, Kueneman J, McKenzie V. (2016) Managing amphibian disease with skin microbiota. Trends in Microbiology 24(3): 161 – 164CrossRefPubMed Woodhams DC, Bletz M, Kueneman J, McKenzie V. (2016) Managing amphibian disease with skin microbiota. Trends in Microbiology 24(3): 161 – 164CrossRefPubMed
Metadaten
Titel
Common Cutaneous Bacteria Isolated from Snakes Inhibit Growth of Ophidiomyces ophiodiicola
verfasst von
Aubree J. Hill
Jacob E. Leys
Danny Bryan
Fantasia M. Erdman
Katherine S. Malone
Gabrielle N. Russell
Roger D. Applegate
Heather Fenton
Kevin Niedringhaus
Andrew N. Miller
Matthew C. Allender
Donald M. Walker
Publikationsdatum
13.11.2017
Verlag
Springer US
Erschienen in
EcoHealth / Ausgabe 1/2018
Print ISSN: 1612-9202
Elektronische ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-017-1289-y

Weitere Artikel der Ausgabe 1/2018

EcoHealth 1/2018 Zur Ausgabe

In This Issue

In This Issue