Antonie van Leeuwenhoek

, Volume 109, Issue 8, pp 1167–1175 | Cite as

Isolation of culturable aerobic bacteria and evidence of Kerstersia gyiorum from the blowhole of captive Yangtze finless porpoises

  • Xiaoling Wan
  • Richard William McLaughlin
  • Junying Zhou
  • Yujiang Hao
  • Jinsong ZhengEmail author
  • Ding WangEmail author
Short Communication


Bacterial respiratory illnesses are problematic in aquatic mammals such as the Yangtze finless porpoise (Neophocaena asiaeorientalis asiaeorientalis; YFP), which is now at a critically endangered status. Yet little is known about the bacteria inhabiting the respiratory tract of YFPs. In this study, we preliminarily characterized the culturable aerobic bacteria from blow samples of captive YFPs. The bacterial diversity was assessed through cultivation by direct exhalation onto Columbia blood agar plates and identification of representative isolates through 16S rRNA gene sequence analysis. In total, eleven bacterial species belonging to four phyla Proteobacteria (71 %), Firmicutes (25 %), Bacteroidetes (3 %) and Actinobacteria (1 %) were identified. Most of these isolates were opportunistic pathogens found in respiratory illnesses in humans and animals. We also reported the first case of Kerstersia gyiorum isolated from an animal. This work provides a preliminary assessment of the bacteria present in the respiratory tract of captive YFPs, which will be an important first step in elucidating the roles of normal microbiota in maintaining respiratory health of YFPs. This study also points out the necessity of future long-term monitoring of blowhole microorganisms in the YFPs and making emergency preparedness plans for respiratory tract infections. These measures can aid in assessing the pathogenic risk of the critically endangered YFP populations.


Bacteria Blowhole Kerstersia gyiorum Yangtze finless porpoise 



We are grateful to the trainers of Wuhan Baiji Dolphinarium for collecting blowhole samples. Special gratitude to Dr. William Wade and the anonymous reviewers for their valuable suggestions for improving the manuscript. This work was supported by grants from the National Natural Science Foundation of China (Nos. 31430080 and 31000168), the Experimental Platform Program of the Chinese Academy of Sciences (No. CZBZX-1), and the Special Conservation Fund for the Yangtze finless porpoise from the Ministry of Agriculture of China.

Compliance with ethical standards

See Methods

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10482_2016_713_MOESM1_ESM.doc (176 kb)
Supplementary material 1 (DOC 176 kb)


  1. Acevedo-Whitehouse K, Rocha-Gosselin A, Gendron D (2010) A novel non-invasive tool for disease surveillance of free-ranging whales and its relevance to conservation programs. Anim Conserv 13:217–225CrossRefGoogle Scholar
  2. Almuzara MN, Barberis CM, Traglia GM, Ordoñez AM, Famiglietti AM, Ramirez MS, Vay CA (2012) Isolation of Kerstersia gyiorum from a patient with cholesteatomatous chronic otitis media. J Clin Microbiol 50:3809–3811CrossRefPubMedPubMedCentralGoogle Scholar
  3. Avalos-Téllez R, Suárez-Güemes F, Carrillo-Casas E, Hernández-Castro R, Méndez-Vilas A (2010) Bacteria and yeast normal microbiota from respiratory tract and genital area of bottlenose dolphins (Tursiops truncatus). Curr Res Technol Educ Top Appl Microbiol Microbial Biotechnol Microbiol Ser 2:666–673Google Scholar
  4. Bostwick AD, Zhang C, Manninen K, Touchberry J, Greene SR, Holland TL (2015) Bacteremia caused by Kerstersia gyiorum. J Clin Microbiol 53:1965–1967CrossRefPubMedPubMedCentralGoogle Scholar
  5. Buck JD, Bubucis PM, Spotte S (1988) Microbiological characterization of three Atlantic whiteside dolphins (Lagenorhynchus acutus) from stranding through captivity with subsequent rehabilitation and release of one animal. Zoo Biol 7:133–138CrossRefGoogle Scholar
  6. Buenviaje G, Ladds P, Melville L, Manolis S (1994) Disease–husbandry associations in farmed crocodiles in Queensland and the Northern Territory. Aust Vet J 71:165–173CrossRefPubMedGoogle Scholar
  7. Camus A, Hawke J (2002) Providencia rettgeri-associated septicemia and meningoencephalitis in juvenile farmed American alligators Alligator mississippiensis. J Aquat Anim Health 14:149–153CrossRefGoogle Scholar
  8. Coenye T, Vancanneyt M, Cnockaert MC, Falsen E, Swings J, Vandamme P (2003) Kerstersia gyiorum gen. nov., sp. nov., a novel Alcaligenes faecalis-like organism isolated from human clinical samples, and reclassification of Alcaligenes denitrificans Rüger and Tan 1983 as Achromobacter denitrificans comb. nov. Int J Syst Evol Micr 53:1825–1831CrossRefGoogle Scholar
  9. Couto I, Sanches IS, Sá-Leão R, de Lencastre H (2000) Molecular characterization of Staphylococcus sciuri strains isolated from humans. J Clin Microbiol 38:1136–1143PubMedPubMedCentralGoogle Scholar
  10. Cox H, Hoskins J, Newman S, Foil C, Turnwald G, Roy A (1988) Temporal study of Staphylococcal species on healthy dogs. Am J Vet Res 49:747–751PubMedGoogle Scholar
  11. Cusick P, Bullock B (1973) Ulcerative dermatitis and pneumonia associated with Aeromonas hydrophila infection in the bottle-nosed dolphin. J Am Vet Med Assoc 163:578PubMedGoogle Scholar
  12. da Silva PSL, Pereira GH (2013) Elizabethkingia meningoseptica: emergent bacteria causing pneumonia in a critically ill child. Pediatr Int 55:231–234CrossRefPubMedGoogle Scholar
  13. Deutscher M, Severing J, Balada-Llasat J-M (2014) Kerstersia gyiorum isolated from a bronchoalveolar lavage in a patient with a chronic tracheostomy. Case Rep Infect Dis 2014:479581. doi: 10.1155/2014/479581 PubMedPubMedCentralGoogle Scholar
  14. Domingo P, Muñoz R, Frontera G, Pericas R, Martinez E (1995) Community-acquired pneumonia due to Acinetobacter lwoffii in a patient infected with the human immunodeficiency virus. Clin Infect Dis 20:205–206CrossRefPubMedGoogle Scholar
  15. Dunn J, Buck J, Robeck T (2001) Bacterial diseases of cetaceans and pinnipeds. CRC Handb Mar Mammal Med 2:309–335Google Scholar
  16. Hedin G, Widerström M (1998) Endocarditis due to Staphylococcus sciuri. Eur J Clin Microbiol 17:673–675Google Scholar
  17. Jefferson TA, Wang JY (2011) Revision of the taxonomy of finless porpoises (genus Neophocaena): the existence of two species. J Mar Anim Ecol 4:3–16Google Scholar
  18. Johnson WR, Torralba M, Fair PA, Bossart GD, Nelson KE, Morris PJ (2009) Novel diversity of bacterial communities associated with bottlenose dolphin upper respiratory tracts. Env Microbiol Rep 1:555–562CrossRefGoogle Scholar
  19. Kolawole D, Shittu A (1997) Unusual recovery of animal staphylococci from septic wounds of hospital patients in Ile-Ife, Nigeria. Lett Appl Microbiol 24:87–90CrossRefPubMedGoogle Scholar
  20. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol. doi: 10.1093/molbev/msw054 Google Scholar
  21. Kyung Y, Kwon O (2011) Two cases of bacterial pneumonia in bottle-nosed dolphins (Tursiops gillii) at the Seoul Zoo, Korea. Pak Vet J 31:260–262Google Scholar
  22. Ladds P, Bradley J, Hirst R (1996) Providencia rettgeri meningitis in hatchling saltwater crocodiles (Crocodylus porosus). Aust Vet J 74:397–398CrossRefPubMedGoogle Scholar
  23. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics:125-175Google Scholar
  24. Lima N, Rogers T, Acevedo-Whitehouse K, Brown MV (2012) Temporal stability and species specificity in bacteria associated with the bottlenose dolphins respiratory system. Env Microbiol Rep 4:89–96CrossRefGoogle Scholar
  25. Morris PJ, Johnson WR, Pisani J, Bossart GD, Adams J, Reif JS, Fair PA (2011) Isolation of culturable microorganisms from free-ranging bottlenose dolphins (Tursiops truncatus) from the southeastern United States. Vet Microbiol 148:440–447CrossRefPubMedGoogle Scholar
  26. Mwalutende A et al (2014) Two cases of chronic suppurative otitis media caused by Kerstersia gyiorum in Tanzania: is it an underappreciated pathogen in chronic otitis media? Int J Infect Dis 29:251–253CrossRefPubMedGoogle Scholar
  27. Pence MA, Sharon J, Tekippe EM, Pakalniskis BL, Ford BA, Burnham C-AD (2013) Two cases of Kerstersia gyiorum isolated from sites of chronic infection. J Clin Microbiol 51:2001–2004CrossRefPubMedPubMedCentralGoogle Scholar
  28. Schroeder P et al. (2009) Investigation into the microbial culture and molecular screening of exhaled breaths of endangered southern resident killer whales (SRKW) and pathogen screening of the seasurface microlayer (SML) in Puget Sound. Report to the Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, SeattleGoogle Scholar
  29. Silvanose C, Bailey T, Naldo J, Howlett J (2001) Bacterial flora of the conjunctiva and nasal cavity in normal and diseased captive bustards. Avian Dis 45:447–451CrossRefPubMedGoogle Scholar
  30. Smith K, Acevedo-whitehouse K, Pedersen AB (2009) The role of infectious diseases in biological conservation. Anim Conserv 12:1–12CrossRefGoogle Scholar
  31. Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Micr 44(4):846–849CrossRefGoogle Scholar
  32. Sweeney J, Ridgway S (1975) Common diseases of small cetaceans. J Am Vet Med Assoc 167:533–540PubMedGoogle Scholar
  33. Swenshon M, LaÈmmler C, Siebert U (1998) Identification and molecular characterization of β-hemolytic streptococci isolated from harbor porpoises (Phocoena phocoena) of the North and Baltic Seas. J Clin Microbiol 36:1902–1906PubMedPubMedCentralGoogle Scholar
  34. Tayeb LA, Lefevre M, Passet V, Diancourt L, Brisse S, Grimont PA (2008) Comparative phylogenies of Burkholderia, Ralstonia, Comamonas, Brevundimonas and related organisms derived from rpoB, gyrB and rrs gene sequences. Res Microbiol 159:169–177CrossRefPubMedGoogle Scholar
  35. Tindall BJ, Rosselló-Mora R, Busse HJ, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Micr 60(1):249–266CrossRefGoogle Scholar
  36. Vandamme P, De Brandt E, Houf K, De Baere T (2012) Kerstersia similis sp. nov., isolated from human clinical samples. Int J Syst Evol Micr 62:2156–2159CrossRefGoogle Scholar
  37. Vergara-Parente JE, Sidrim JJC, de Pinho Pessoa ABG, Parente CL, Marcondes MCC, da Silva Teixeira MF, Rocha MFG (2003) Bacterial flora of upper respiratory tract of captive Antillean manatees. Aquat Mammals 29:124–130CrossRefGoogle Scholar
  38. Wallet F, Stuit L, Boulanger E, Roussel-Delvallez M, Dequiedt P, Courcol RJ (2000) Peritonitis due to Staphylococcus sciuri in a patient on continuous ambulatory peritoneal dialysis. Scand J Infect Dis 32:697–698CrossRefPubMedGoogle Scholar
  39. Wang D, Hao Y, Wang K, Zhao Q, Chen D, Wei Z, Zhang X (2005) Aquatic resource conservation: the first Yangtze finless porpoise successfully born in captivity. Environ Sci Pollut R 12:247–250CrossRefGoogle Scholar
  40. Wang J, Frasier T, Yang S, White B (2008) Detecting recent speciation events: the case of the finless porpoise (genus Neophocaena). Heredity 101:145–155CrossRefPubMedGoogle Scholar
  41. Wang D, Turvey S, Zhao X, Mei Z (2013) Neophocaena asiaeorientalis ssp. Asiaeorientalis. IUCN Red List of Threatened Species Version 2013Google Scholar
  42. Welk S (1982) Achromobacter pneumonia. W J Med 136:349Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Xiaoling Wan
    • 1
    • 2
  • Richard William McLaughlin
    • 1
    • 3
  • Junying Zhou
    • 4
  • Yujiang Hao
    • 1
  • Jinsong Zheng
    • 1
    Email author
  • Ding Wang
    • 1
    Email author
  1. 1.The Key Laboratory of Aquatic Biodiversity and Conservation of the Chinese Academy of Sciences, Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Biology DepartmentSaint Mary’s University of MinnesotaWinonaUSA
  4. 4.ZhongNan Hospital of Wuhan UniversityWuhanChina

Personalised recommendations