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Bacterial and Viral Diversity of Didelphid Opossums from Brazil

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Abstract

Marsupials belonging to the Didelphis genus are widely distributed in the American Continent, and Didelphis albiventris and Didelphis aurita, are common in all of their areas of distribution in Brazil. Here we describe the bacterial and viral diversity of samples from opossums captured in three forest fragments in the State of São Paulo, Brazil. Microbiomes from the same body site were more similar across species and sampling sites while oral swabs presented higher bacterial diversity than rectal swabs. We also identified sequences related to bacterial species involved in zoonotic diseases. The detection of pathogens in such abundant mammal species warns for the possibility of emergence in other species.

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Data Availability

These sequencing data have been submitted to the SRA repository, under bioproject PRJNA613851.

References

  • Anindita PD, Sasaki M, Gonzalez G, Phongphaew W, Carr M, Hang BM, Mweene AS, Ito K (2019) Discovery and genetic characterization of diverse smacoviruses in Zambian non- human primates. 1–10 . https://doi.org/10.1038/s41598-019-41358-z

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  MathSciNet  PubMed  PubMed Central  CAS  Google Scholar 

  • Barrett ADT, Stanberry LR, Sarkar-Tyson M, Titball RW (2009) Burkholderia mallei and Burkholderia pseudomallei. Vaccines Biodefense Emerg Neglected Dis 831–843 . https://doi.org/10.1016/B978-0-12-369408-9.00043-3

  • Barron MC, Pech RP, Whitford J, Yockney IJ, De Lisle GW, Nugent G (2011) New Zealand Veterinary Journal Longevity of Mycobacterium bovis in brushtail possum (Trichosurus vulpecula) carcasses, and contact rates between possums and carcasses Longevity of Mycobacterium bovis in brushtail possum (Trichosurus vulpecula) carcasses, and contact rates between possums and carcasses. https://doi.org/10.1080/00480169.2011.595905

  • Bjorklund B, Haley B, Bevilacqua R, Chandler M, Duffiney A, von Hone K, Slate D, Chipman R, Martin A, Algeo T (2017) Progress towards Bait Station Integration into Oral Rabies Vaccination Programs in the United States: Field Trials in Massachusetts and Florida. Trop Med Infect Dis 2:40. https://doi.org/10.3390/tropicalmed2030040

    Article  PubMed  PubMed Central  Google Scholar 

  • Bondo KJ, Pearl DL, Janecko N, Reid‐Smith RJ, Parmley EJ, Weese JS, Rousseau J, Taboada E, Mutschall S, Jardine CM (2019) Salmonella , Campylobacter , Clostridium difficile , and anti‐microbial resistant Escherichia coli in the faeces of sympatric meso‐mammals in southern Ontario, Canada. Zoonoses Public Health zph.12576 . https://doi.org/10.1111/zph.12576

  • Cáceres NC (2000) Population ecology and reproduction of the white-eared opossum Didelphis albiventris (Mammalia, Marsupialia) in an urban environment of Brazil. Cienc Cult 52:171–174

    Google Scholar 

  • Cáceres NC, Monteiro-Filho ELA (2003) Food Habits, Home Range and Activity of Didelphis aurita (Mammalia, Marsupialia) in a Forest Fragment of Southern Brazil. Stud Neotrop Fauna Environ 36:85–92. https://doi.org/10.1076/snfe.36.2.85.2138

    Article  Google Scholar 

  • Carneiro IDO, Sander A, Silva N, Moreira-soto A, Normann A, Flehmig B (2018) crossm. 92:1–14

  • de Almeida AJ, Torquetti CG, Talamoni SA (2008) Use of space by neotropical marsupial Didelphis albiventris (Didelphimorphia: Didelphidae) in an urban forest fragment. Rev Bras Zool 25:214–219. https://doi.org/10.1590/s0101-81752008000200008

    Article  Google Scholar 

  • De Araujo J, Thomazelli LM, Henriques DA, Lautenschalager D, Ometto T, Dutra LM, Aires CC, Favorito S, Durigon EL (2012) Detection of hantavirus in bats from remaining rain forest in São Paulo. Brazil. BMC Res Notes 5:1. https://doi.org/10.1186/1756-0500-5-690

    Article  Google Scholar 

  • de Souza WM, Fumagalli MJ, de Araujo J, Sabino-Santos G, Maia FGM, Romeiro MF, Modha S, Nardi MS, Queiroz LH, Durigon EL, Nunes MRT, Murcia PR, Figueiredo LTM (2018) Discovery of novel anelloviruses in small mammals expands the host range and diversity of the Anelloviridae. Virology 514:9–17. https://doi.org/10.1016/j.virol.2017.11.001

    Article  PubMed  CAS  Google Scholar 

  • DeVault TL, Olson ZH, Beasley JC, Rhodes OE (2011) Mesopredators dominate competition for carrion in an agricultural landscape. Basic Appl Ecol 12:268–274. https://doi.org/10.1016/j.baae.2011.02.008

    Article  Google Scholar 

  • Dias CAR, Perini FA (2018) Biogeography and early emergence of the genus Didelphis (Didelphimorphia, Mammalia). Zool Scr 47:645–654. https://doi.org/10.1111/zsc.12306

    Article  Google Scholar 

  • Dos Reis, N. R.; Peracchi, A.l.; Pedro, W. A.; Lima IP (2006) Ordem Didelphimorphia. In: Mamíferos do Brasil.

  • Eisenhofer R, D’Agnese E, Taggart D, Carver S, Penrose B (2022) Microbial biogeography of the wombat gastrointestinal tract. PeerJ 10:1–19. https://doi.org/10.7717/peerj.12982

    Article  CAS  Google Scholar 

  • Gómez A, Kilpatrick AM, Kramer LD, Dupuis AP, Maffei JG, Marra PP, Daszak P, Aguirre AA (2008) Multiple factors influence West Nile virus seroprevalence in wild mammals. Emerg Infect Dis 14:962–965

    Article  PubMed  PubMed Central  Google Scholar 

  • Hansen MJ, Bertelsen MF, Kelly A, Bojesen AM (2017) Occurrence Of Pasteurellaceae Bacteria In The Oral Cavity Of Selected Marsupial Species. J Zoo Wildl Med off Publ Am Assoc Zoo Vet 48:1215–1218. https://doi.org/10.1638/2017-0071.1

    Article  Google Scholar 

  • Kayesh MEH, Hashem MA, Tsukiyama-Kohara K (2020) Koala retrovirus epidemiology, transmission mode, pathogenesis, and host immune response in koalas (Phascolarctos cinereus): a review. Arch Virol 165:2409–2417. https://doi.org/10.1007/s00705-020-04770-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 7:11257

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  • Ng TFF, Zhang W, Sachsenröder J, Kondov NO, da Costa AC, Vega E, Holtz LR, Wu G, Wang D, Stine CO, Antonio M, Mulvaney US, Muench MO, Deng X, Ambert-Balay K, Pothier P, Vinjé J, Delwart E (2015) A diverse group of small circular ssDNA viral genomes in human and non-human primate stools. Virus Evol 1:vev017–vev017 . https://doi.org/10.1093/ve/vev017

  • Ogden ID, Dallas JF, MacRae M, Rotariu O, Reay KW, Leitch M, Thomson AP, Sheppard SK, Maiden M, Forbes KJ, Strachan NJC (2009) Campylobacter excreted into the environment by animal sources: prevalence, concentration shed, and host association. Foodborne Pathog Dis 6:1161–1170. https://doi.org/10.1089/fpd.2009.0327

    Article  PubMed  Google Scholar 

  • Olival KJ, Weekley CC, Daszak P (2015) Are Bats Really “Special” as Viral Reservoirs? What We Know and Need to Know. Bats Viruses A New Front Emerg Infect Dis 281–294 . https://doi.org/10.1002/9781118818824.ch11

  • Olson ZH, Beasley JC, Rhodes OE Jr (2016) Carcass Type Affects Local Scavenger Guilds More than Habitat Connectivity. PLoS One 11:e0147798

    Article  PubMed  PubMed Central  Google Scholar 

  • Olvera-Ramírez AM, McEwan NR, Stanley K, Nava-Diaz R, Aguilar-Tipacamú G (2023) A Systematic Review on the Role of Wildlife as Carriers and Spreaders of Campylobacter spp. Animals 13

  • Peres MG, Bacchiega TS, Appolinário CM, Vicente AF, Mioni M de SR, Ribeiro BLD, Fonseca CRS, Pelícia VC, Ferreira F, Oliveira GP, Abrahão JS, Megid J (2018) Vaccinia virus in blood samples of humans, domestic and wild mammals in Brazil. Viruses 10:1–12 . https://doi.org/10.3390/v10010042

  • Robertson CE, Harris JK, Wagner BD, Granger D, Browne K, Tatem B, Feazel LM, Park K, Pace NR, Frank DN (2013) Explicet: graphical user interface software for metadata-driven management, analysis and visualization of microbiome data. Bioinformatics 29:3100–3101. https://doi.org/10.1093/bioinformatics/btt526

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rowena C, Mang S, E. GC, C. HE, J. HC, Katherine B, R. BV (2019) Fecal Viral Diversity of Captive and Wild Tasmanian Devils Characterized Using Virion-Enriched Metagenomics and Metatranscriptomics. J Virol 93:https://doi.org/10.1128/jvi.00205-19 . https://doi.org/10.1128/jvi.00205-19

  • Ryan JR (2016) Chapter 4 - Category B Diseases and Agents. In: Ryan JRBT-B and B (Second E (ed). Butterworth-Heinemann, pp 85–111

  • Soc PRB, Fooks CE, Rupprecht JLN, Wood CTW, Pulliam JN, Mills ME, Timonin CKR, Willis AA, Cunningham AR, Angela D, Luis DTS, Hayman TJ, O ’shea PM, Cryan AT, Gilbert JRC, Luis AD, Hayman DTS, O ’shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, Mills JN, Timonin ME, Willis CKR, Cunningham AA, Fooks AR, Rupprecht CE, Wood JLN, Webb CT (2012) viruses: are bats special? A comparison of bats and rodents as reservoirs of zoonotic A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc R Soc B

  • Stearns JC, Lynch MDJ, Senadheera DB, Tenenbaum HC, Goldberg MB, Cvitkovitch DG, Croitoru K, Moreno-Hagelsieb G, Neufeld JD (2011) Bacterial biogeography of the human digestive tract. Sci Rep 1:170. https://doi.org/10.1038/srep00170

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  • Strauss JH, Strauss EG (2008) Viruses Whose Life Cycle Uses Reverse Transcriptase. In: Viruses and Human Disease. Academic Press, pp 211–259

  • Temmam S, Davoust B, Berenger JM, Raoult D, Desnues C (2014) Viral metagenomics on animals as a tool for the detection of zoonoses prior to human infection? Int J Mol Sci 15:10377–10397. https://doi.org/10.3390/ijms150610377

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Torkan S, Vazirian B, Khamesipour F, Dida GO (2018) Prevalence of thermotolerant Campylobacter species in dogs and cats in Iran. Vet Med Sci 4:296–303 . https://doi.org/10.1002/vms3.117

  • Walter WD, Fischer JW, Anderson CW, Marks DR, Deliberto T, Robbe-Austerman S, Vercauteren KC (2013) Surveillance and movements of Virginia opossum (Didelphis virginiana) in the bovine tuberculosis region of Michigan. Epidemiol Infect 1498 . https://doi.org/10.1017/S0950268813000629 (2019) Google Earth Pro

  • (2019) Google Earth Pro

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Acknowledgements

We would like to thank Brazilian Bioethanol Science and Technology Laboratory CNPEM/MCTIC NGS Sequencing Facility for generating the sequencing data described here. We also thank Thomaz Henrique Barrella (Fundação José Pedro de Oliveira, Mata de Santa Genebra), Márcia Gonçalves Rodrigues (ICMBio) and Angela Podolsky for providing access to the forest fragments and help in fieldwork. This work was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil (Grant Number 870370/1997-9 and scholarship number 154978/2016-7). This work was also financed in part by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil—Finance Code 001 and Fundação de Amparo à pesquisa do Estado de São Paulo (FAPESP), Brazil (Grant Number 2014/50696-4).

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Correspondence to Leonardo Cardia Caserta.

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Cardia Caserta, L., Mansano do Nascimento, G., Joshi, L.R. et al. Bacterial and Viral Diversity of Didelphid Opossums from Brazil. EcoHealth 20, 362–369 (2023). https://doi.org/10.1007/s10393-023-01667-2

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