Skip to main content

Advertisement

SpringerLink
Log in

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

  • Short Communication
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • 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 13:217–225

    Article  Google Scholar 

  • 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 50:3809–3811

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 2:666–673

    Google Scholar 

  • Bostwick AD, Zhang C, Manninen K, Touchberry J, Greene SR, Holland TL (2015) Bacteremia caused by Kerstersia gyiorum. J Clin Microbiol 53:1965–1967

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 7:133–138

    Article  Google Scholar 

  • Buenviaje G, Ladds P, Melville L, Manolis S (1994) Disease–husbandry associations in farmed crocodiles in Queensland and the Northern Territory. Aust Vet J 71:165–173

    Article  CAS  PubMed  Google Scholar 

  • Camus A, Hawke J (2002) Providencia rettgeri-associated septicemia and meningoencephalitis in juvenile farmed American alligators Alligator mississippiensis. J Aquat Anim Health 14:149–153

    Article  Google Scholar 

  • 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 53:1825–1831

    Article  CAS  Google Scholar 

  • Couto I, Sanches IS, Sá-Leão R, de Lencastre H (2000) Molecular characterization of Staphylococcus sciuri strains isolated from humans. J Clin Microbiol 38:1136–1143

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 49:747–751

    CAS  PubMed  Google Scholar 

  • Cusick P, Bullock B (1973) Ulcerative dermatitis and pneumonia associated with Aeromonas hydrophila infection in the bottle-nosed dolphin. J Am Vet Med Assoc 163:578

    CAS  PubMed  Google Scholar 

  • da Silva PSL, Pereira GH (2013) Elizabethkingia meningoseptica: emergent bacteria causing pneumonia in a critically ill child. Pediatr Int 55:231–234

    Article  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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 20:205–206

    Article  CAS  PubMed  Google Scholar 

  • Dunn J, Buck J, Robeck T (2001) Bacterial diseases of cetaceans and pinnipeds. CRC Handb Mar Mammal Med 2:309–335

    Google Scholar 

  • Hedin G, Widerström M (1998) Endocarditis due to Staphylococcus sciuri. Eur J Clin Microbiol 17:673–675

    CAS  Google Scholar 

  • Jefferson TA, Wang JY (2011) Revision of the taxonomy of finless porpoises (genus Neophocaena): the existence of two species. J Mar Anim Ecol 4:3–16

    Google Scholar 

  • 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 1:555–562

    Article  CAS  Google Scholar 

  • Kolawole D, Shittu A (1997) Unusual recovery of animal staphylococci from septic wounds of hospital patients in Ile-Ife, Nigeria. Lett Appl Microbiol 24:87–90

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Kyung Y, Kwon O (2011) Two cases of bacterial pneumonia in bottle-nosed dolphins (Tursiops gillii) at the Seoul Zoo, Korea. Pak Vet J 31:260–262

    Google Scholar 

  • Ladds P, Bradley J, Hirst R (1996) Providencia rettgeri meningitis in hatchling saltwater crocodiles (Crocodylus porosus). Aust Vet J 74:397–398

    Article  CAS  PubMed  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics:125-175

  • 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 4:89–96

    Article  Google Scholar 

  • 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 148:440–447

    Article  PubMed  Google Scholar 

  • 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 29:251–253

    Article  PubMed  Google Scholar 

  • 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 51:2001–2004

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, Seattle

  • 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 45:447–451

    Article  CAS  PubMed  Google Scholar 

  • Smith K, Acevedo-whitehouse K, Pedersen AB (2009) The role of infectious diseases in biological conservation. Anim Conserv 12:1–12

    Article  Google Scholar 

  • 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):846–849

    Article  CAS  Google Scholar 

  • Sweeney J, Ridgway S (1975) Common diseases of small cetaceans. J Am Vet Med Assoc 167:533–540

    CAS  PubMed  Google Scholar 

  • 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 36:1902–1906

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 159:169–177

    Article  CAS  PubMed  Google Scholar 

  • 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):249–266

    Article  CAS  Google Scholar 

  • 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 62:2156–2159

    Article  Google Scholar 

  • 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 29:124–130

    Article  Google Scholar 

  • 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 32:697–698

    Article  CAS  PubMed  Google Scholar 

  • 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 12:247–250

    Article  Google Scholar 

  • Wang J, Frasier T, Yang S, White B (2008) Detecting recent speciation events: the case of the finless porpoise (genus Neophocaena). Heredity 101:145–155

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Turvey S, Zhao X, Mei Z (2013) Neophocaena asiaeorientalis ssp. Asiaeorientalis. IUCN Red List of Threatened Species Version 2013

  • Welk S (1982) Achromobacter pneumonia. W J Med 136:349

    CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. The Key Laboratory of Aquatic Biodiversity and Conservation of the Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, No. 7 Donghu South Road, Wuhan, 430072, China

    Xiaoling Wan, Richard William McLaughlin, Yujiang Hao, Jinsong Zheng & Ding Wang

  2. University of Chinese Academy of Sciences, Beijing, 100039, China

    Xiaoling Wan

  3. Biology Department, Saint Mary’s University of Minnesota, 700 Terrace, Winona, MN, 55987-1399, USA

    Richard William McLaughlin

  4. ZhongNan Hospital of Wuhan University, Wuhan, 430072, China

    Junying Zhou

Authors
  1. Xiaoling Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard William McLaughlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junying Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yujiang Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinsong Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ding Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jinsong Zheng or Ding Wang.

Ethics declarations

See Methods

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 176 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wan, X., McLaughlin, R.W., Zhou, J. et al. Isolation of culturable aerobic bacteria and evidence of Kerstersia gyiorum from the blowhole of captive Yangtze finless porpoises. Antonie van Leeuwenhoek 109, 1167–1175 (2016). https://doi.org/10.1007/s10482-016-0713-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-016-0713-6

Keywords

Search

Navigation