Bacterial and fungal pathogens in granulomatous lesions of Chelonia mydas in a significant foraging ground off southern Brazil

Veterinary Research Communications - Tập 46 - Trang 859-870 - 2022
Isabela Guarnier Domiciano1, Gabrielle Fernanda Pereira da Silva Gagliotti1, Camila Domit2, Elis Lorenzetti3,4, Ana Paula Frederico Rodrigues Loureiro Bracarense1
1Laboratory of Animal Pathology, Department of Preventive Veterinary Medicine, Universidade Estadual de Londrina, Londrina, Brazil
2Laboratory of Ecology and Conservation, Paraná Federal University, Pontal do Paraná, Brazil
3Laboratory of Animal Virology, Universidade Estadual de Londrina, Londrina, Brazil
4Post Graduate Program in Animal Health and Production, Pitágoras Unopar University, Londrina, Brazil

Tóm tắt

The green sea turtle Chelonia mydas inhabit near-shore areas exposed to threatening anthropogenic activities. The granulomatous lesions in these animals may indicate infectious diseases that can be associated with environmental contamination and hazards to human health. This study aimed to characterize the granulomatous inflammation associated with bacterial and fungal infection in C. mydas off Paraná state. From September 2015 to February 2019, systematic monitoring was performed by the Santos Basin Beach Monitoring Project for sea turtles’carcasses recovery, necropsy, and cause of death diagnosis. The tissue samples were fixed in buffered formalin 10% for histochemical analysis and frozen for molecular analysis to fungi detection (Internal Transcribed Spacer region of the nuclear rDNA) and bacteria detection (16S ribosomal gene). From a total of 270 C. mydas, granulomatous lesions were observed in different organs of 63 (23.3%) individuals. The histological analysis indicated lesions in 94 organs, affecting most respiratory and digestive systems. Bacteria were identified in 25 animals, including an acid-fast bacteria detected in one animal, and fungi in 24 C. mydas. The fungi species included the genus Candida (Candida zeylanoides, n = 3), Yarrowia (Yarrowia lipolytica, n = 9; Yarrowia deformans, n = 5; and Yarrowia divulgata, n = 1), and Cladosporium anthropophilum (n = 1). No species of bacteria was identified by molecular testing. All fungi species identified are saprobic, some are important to food and medical industries, but are also pathogens of humans and other animals. Therefore, long-term monitoring of these pathogens and the C. mydas health may indicate changes in environmental quality, possible zoonotic diseases, and their effects.

Tài liệu tham khảo

Andrade MF, Domit C, Broadhurst MK, Tolhurst DJ, Silva Souza ÂT (2016) Appropriate morphometrics for the first assessment of juvenile green turtle (Chelonia mydas) age and growth in the South-Western Atlantic. Mar Biol 163:254. https://doi.org/10.1007/s00227-016-3031-7 Arshad H, Garcia S, Khaja M (2017) Case report of invasive, disseminated candidiasis with peripheral nodular cavitary lesions in the lung. Respir Med Case Rep. https://doi.org/10.1016/j.rmcr.2016.11.003 Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol. https://doi.org/10.3114/sim0003 Bjorndal KA, Bolten AB (1989) Comparison of straight-line and over-the-curve measurements for growth rates of green turtles, Chelonia mydas. Bull Mar Sci 45:189–192 Brock JA, Nakamura RM, Miyahara AY, Chang EML (1976) Tuberculosis in Pacific green sea turtles, Chelonia mydas. Trans Am Fish Soc. https://doi.org/10.1577/1548-8659(1976)105<564:TIPGST>2.0.CO;2 Chang C-F, Lee C-F, Lin K-Y, Liu S-M (2016) Diversity of yeasts associated with the sea surface microlayer and underlying water along the northern coast of Taiwan. Res Microbiol. https://doi.org/10.1016/j.resmic.2015.08.005 Chapman PA, Cribb TH, Flint M, Traub RJ, Blair D, Kyaw-Tanner MT, Mills PC (2019) Spirorchiidiasis in marine turtles: the current state of knowledge. Dis Aquat Org. https://doi.org/10.3354/dao03348 Chuen-Im T, Areekijseree M, Chongthammakun S, Graham SV (2010) Aerobic bacterial infections in captive juvenile green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) from Thailand. Chelonian Conserv Biol. https://doi.org/10.2744/CCB-0808.1 Coelho VF, Domit C, Broadhurst MK, Prosdocimi L, Nishizawa H, Almeida FS (2018) Intra-specific variation in skull morphology of juvenile Chelonia mydas in the southwestern Atlantic Ocean. Mar Biol. https://doi.org/10.1007/s00227-018-3429-5 Crozier WJ (1993) Two cases of onychomycoses due to Candida zeylanoides. Aust J Dermatol. https://doi.org/10.1111/j.1440-0960.1993.tb00842.x Cruz LCH (2010) Candida. In: Micologia Veterinária, 2nd edn. Revinter, Rio de Janeiro, pp 163–178 Domiciano IG, Domit C, Bracarense APFRL (2017) The green turtle Chelonia mydas as a marine and coastal environmental sentinels: anthropogenic activities and diseases. Ciênc Agrá, Semina. https://doi.org/10.5433/1679-0359.2017v38n5p3417 Dorko E, Pilipčinec E, Tkáčiková L (2002) Fungal diseases of the respiratory tract. Folia Microbiol. https://doi.org/10.1007/BF02817657 Ebani VV (2017) Domestic reptiles as source of zoonotic bacteria: a mini review. Asian Pac J Trop Med. https://doi.org/10.1016/j.apjtm.2017.07.020 Flint M, Petterson-Kane JC, Limpus CJ, Mills PC (2010) Health surveillance of stranded green turtles in southern Queensland, Australia (2006–2009): an epidemiological analysis of causes of disease and mortality. Ecohealth. https://doi.org/10.1007/s10393-010-0300-7 Fuentes MMPB, Wildermann N, Gandra TBR, Domit C (2020) Cumulative threats to juvenile green turtles in the coastal waters of southern and southeastern Brazil. Biodivers Conserv. https://doi.org/10.1007/s10531-020-01964-0 Geraci JR, Lounsbury VJ (2005) Marine mammals ashore: a field guide for strandings. National Aquarium in Baltimore, Baltimore Glazebrook JS, Campbell RSF (1990) A survey of the diseases of marine turtles in northern Australia, I. farmed turtles. Dis Aquat Org 9:83–95 Goldberg DW, Fernandes MR, Sellera FP, Costa DGC, Bracarense APFRL, Lincopan N (2019) Genetic background of CTX-M-15 producing Enterobacter hormaechei ST114 and Citrobacter freundii ST265 co-infecting a free-living green turtle (Chelonia mydas). Zoonoses Public Health. https://doi.org/10.1111/zph.12572 Gordon AN, Kelly WR, Cribb TH (1998) Lesions caused by cardiovascular flukes (Digenea: Spirorchidae) in stranded green turtles (Chelonia mydas). Vet Pathol. https://doi.org/10.1177/030098589803500102 Groenewald M, Smith MT (2013) The teleomorph state of Candida deformans Langeron & Guerra and description of Yarrowia yakushimensis comb. nov. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-013-9882-8 Groenewald M, Boekhout T, Neuvéglise C, Gaillardin C, van Dijck PWM, Wyss M (2013) Yarrowia lipolytica: safety assessment of an oleaginous yeast with a great industrial potential. Crit Rev Microbiol. https://doi.org/10.3109/1040841X.2013.770386 Hargrove S, Work T, Brunson S, Foley AM, Balazs G (2016) Proceedings of the 2015 international summit on fibropapillomatosis: global status, trends, and population impacts. NOAA Technical Memorandum, NOAA-TM-NMFS-PIFSC-54. https://doi.org/10.7289/V5/TM-PIFSC-54 Homer BL, Jacobson ER, Schumacher J, Scherba G (1994) Chlamydiosis in mariculture-reared green sea turtles. Vet Pathol. https://doi.org/10.1177/030098589403100101 Innis C, Nyaoke AC, Williams CR III, Dunnigan B, Merigo C, Woodward DL, Weber ES, Frasca S Jr (2009) Pathologic and parasitologic findings of cold-stunned Kemp’s Ridley Sea turtles (Lepidochelys kempii) stranded on Cape Cod, Massachusetts, 2001–2006. J Wildl Dis. https://doi.org/10.7589/0090-3558-45.3.594 IUCN (2022) Chelonia mydas. The IUCN Red List of Threatened Species. Version 2021.3. https://www.iucnredlist.org/species/4615/11037468 Accessed 6 February 2022 Jacobson ER, Gaskin JM, Shields RP, White FH (1979) Mycotic pneumonia in mariculture-reared green sea turtle. J Am Vet Med Assoc 175:929–933 Jacobson ER, Gaskin JM, Roelke M, Greiner EC, Allen J (1986) Conjunctivitis, tracheitis, and pneumonia associated with herpesvirus infection in green sea turtles. J Am Vet Med Assoc 189:1020–1023 Jautová J, Virágová S, Ondrasovic M, Holoda E (2001) Incidence of Candida species isolated from human skin and nails: a survey. Folia Microbiol. https://doi.org/10.1007/bf02815623 Khosravi AR, Shokri H, Nikaein D, Erfanmanesh A, Fatahinia M, Helan JA (2013) Evaluation of the pathogenicity of Candida zeylanoides in BALB/c mice. Turk J Vet Anim Sci. https://doi.org/10.3906/vet-1105-40 Luschi P, Hays GC, Papi F (2003) A review of long-distance movements by marine turtles, and the possible role of ocean currents. Oikos. https://doi.org/10.1034/j.1600-0706.2003.12123.x Montali RJ (1988) Comparative pathology of inflammation in the higher vertebrates (reptiles, birds and mammals). J Comp Pathol. https://doi.org/10.1016/0021-9975(88)90101-6 Mouton M, Reeb D, Botha A, Best P (2009) Yeast infection in a beached southern right whale (Eubalaena australis) neonate. J Wildl Dis. https://doi.org/10.7589/0090-3558-45.3.692 Nagy E, Niss M, Dlauchy D, Arneborg N, Nielsen DS, Péter G (2013) Yarrowia divulgata f.a., sp. nov., a yeast species from animal-related and marine sources. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijs.0.057208-0 Nardoni S, Papini R, Marcucci GM, Mancianti F (2008) Survey on the fungal flora of the cloaca of healthy pet reptiles. Ver Med Vet 159:159–165 Orós J, Calabuig P, Déniz S (2004) Digestive pathology of sea turtles stranded in the Canary Islands between 1993 and 2001. Vet Rec. https://doi.org/10.1136/vr.155.6.169 Orós J, Torrent A, Calabuig P, Déniz S (2005) Diseases and causes of mortality among sea turtles stranded in the Canary Islands, Spain (1998–2001). Dis Aquat Org. https://doi.org/10.3354/dao063013 Pappas PG, Lionakis MS, Arendrup MC, Ostrosky-Zeichner L, Kullberg BJ (2018) Invasive candidiasis. Nat Rev Dis Prim. https://doi.org/10.1038/nrdp.2018.26 Péter G, Nagy ES, Dlauchy D (2019) Systematics, diversity and ecology of the genus Yarrowia and the methanol-assimilating yeasts. In: Sibirny A (ed.) Non-conventional Yeasts: from Basic Research to Application, 1st edn. Springer Nature, pp 297-339. https://doi.org/10.1007/978-3-030-21110-3_9 Raidal SR, Ohara M, Hobbs RP, Prince R (1998) Gram-negative bacterial infections and cardiovascular parasitism in green sea turtles (Chelonia mydas). Aust Vet J. https://doi.org/10.1111/j.1751-0813.1998.tb12392.x Rywinska A, Juszczyk P, Wojtatowicz M, Robak M, Lazar Z, Tomaszewska L, Rymowicz W (2013) Glycerol as a promising substrate for Yarrowia lipolytica biotechnological applications. Biomass Bioenergy. https://doi.org/10.1016/j.biombioe.2012.11.021 Sandoval-Denis M, Gené J, Sutton DA, Wiederhold NP, Cano-Lira JF, Guarro J (2016) New species of Cladosporium associated with human and animal infections. Persoonia 36:281–298. https://doi.org/10.3767/003158516X691951 Santoro M, Mattiucci S (2009) Sea turtle parasites. In: Wehrtmann IS, Cortés J (eds) Marine biodiversity of Costa Rica, Central America, 1st edn. Springer, Costa Rica, pp 507–520 Santoro M, Hernández G, Caballero M, García F (2006) Aerobic bacterial flora of nesting green turtles (Chelonia mydas) from Tortuguero National Park. J Zoo Wild Med, Costa Rica. https://doi.org/10.1638/05-118.1 Santoro M, Morales JA, Rodríguez-Ortíz B (2007) Spirorchiidiosis (Digenea: Spirorchiidae) and lesions associated with parasites in Caribbean green turtles (Chelonia mydas). Vet Rec 161:482–486. https://doi.org/10.1136/vr.161.14.482 Santoro M, Hernandéz G, Caballero M, García F (2008) Potential bacterial pathogens carried by nesting leatherback turtles (Dermochelys coriacea) in Costa Rica. Chelonian Conserv Biol 7(1):104–108 Stacy BA, Pessier AP (2007) Host response to infectious agents and identification of pathogens in tissue section. In: Jacobson ER (ed) Infectious diseases and pathology of reptiles: colour atlas and text. CRC Press, Boca Raton, pp 257–298 Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribossomal DNA amplification for phylogenetic study. J Bacteriol. https://doi.org/10.1128/jb.173.2.697-703.1991 White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322 Work TM, Balazs GH, Wolcott M, Morris R (2003) Bacteraemia in free-ranging Hawaiian green turtles Chelonia mydas with fibropapillomatosis. Dis Aquat Org. https://doi.org/10.3354/dao053041 Work TM, Balazs GH, Summers TM, Hapdei JR, Tagarino AP (2015) Causes of mortality in green turtles from Hawaii and the insular Pacific exclusive of fibropapillomatosis. Dis Aquat Org. https://doi.org/10.3354/dao02890 Zieniuk B, Fabiszewska A (2019) Yarrowia lipolytica: a beneficious yeast in biotechnology as a rare opportunistic fungal pathogen: a minireview. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-018-2583-8