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Environmental Microbiology and Biotechnology (EMB)  |  Microbial Ecology and Diversity

Distributions of Fecal Indicators at Aquaculture Areas in a Bay of Republic of Korea

SungJun Park1,2, Cheonghoon Lee1,3*, Sung Jae Jang1, Kyuseon Cho1, Jin Hwi Kim4, Woon-Ki Kim1,3, Joo-Hyon Kang5, Kwon-Sam Park6, and GwangPyo Ko1,2,3*

1Department of Environmental Health Sciences, Graduate School of Public Health, Seoul National University, Seoul 08826, Republic of Korea
2N-Bio, Seoul National University, Seoul 08826, Republic of Korea
3Institute of Health and Environment, Seoul National University, Seoul 08826, Republic of Korea
4Department of Civil and Environmental Engineering, Konkuk University-Seoul, Seoul 05029, Republic of Korea
5Department of Civil and Environmental Engineering, Dongguk University, Seoul 04620, Republic of Korea
6Department of Food Science and Biotechnology, Kunsan National University, Gunsan 54150, Republic of Korea

Correspondence to:
Cheonghoon Lee,       shota2@snu.ac.kr
GwangPyo Ko,           gko@snu.ac.kr
Received: June 2, 2024; Revised: September 27, 2024; Accepted: October 2, 2024

J. Microbiol. Biotechnol. 2024; 34(11): 2223-2230

Published November 28, 2024 https://doi.org/10.4014/jmb.2406.06001

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Aquaculture products, such as clams, scallops, and oysters, are major vectors of fecal-derived pathogens. Male-specific and somatic coliphages are strongly correlated with human noroviruses, the major enteric viruses worldwide. Geographic information system with local land-use patterns can also provide valuable information for tracking sources of fecal-derived pathogens. We examined distributions of four fecal indicator microorganisms, i.e., male-specific and somatic coliphage, total coliform, and Escherichia coli (E. coli) in three river and seawater sampling sites located on the coast of Gomso Bay in the Republic of Korea during the sampling period (from March 2015 to January 2016). Geospatial analyses of fecal indicators and correlations between environmental parameters and fecal indicators or among fecal indicators were also performed. Overall, river water samples showed highest concentrations of both types of coliphage in summer (July 2015). High concentrations of both total coliform and E. coli were detected in river water during the period from July to September 2015. High concentrations of all fecal indicators were found at site GL02, located in the innermost part of Gomso Bay, which has high-density agriculture and residential areas. Environmental factors related to precipitation—cumulative precipitation on and from 3 days before the sampling day (Prep-0 and Prep-3, respectively)—and salinity were strongly correlated with the concentrations of all fecal indicators. The present results suggest that investigations of multiple fecal indicators with systemic geospatial information are necessary for precisely tracking fecal contaminations of aquaculture products.

Keywords

Fecal contamination, fecal indicator, geographical information system, male-specific coliphage, microbial source tracking, somatic coliphage

Graphical Abstract


References

  1. Iritani N, Kaida A, Abe N, Kubo H, Sekiguchi JI, Yamamoto SP, et al. 2014. Detection and genetic characterization of human enteric viruses in oyster-associated gastroenteritis outbreaks between 2001 and 2012 in Osaka city, Japan. J. Med. Virol. 86: 2019-2025.
    Pubmed
  2. Sutthikornchai C, Popruk S, Chumpolbanchorn K, Sukhumavasi W, Sukthana Y. 2016. Oyster is an effective transmission vehicle for Cryptosporidium infection in human. Asian Pac. J. Trop. Med. 9: 562-566.
    Pubmed
  3. Parveen S, Jacobs J, Ozbay G, Chintapenta LK, Almuhaideb E, Meredith J, et al. 2020. Seasonal and geographical differences in total and pathogenic Vibrio parahaemolyticus and Vibrio vulnificus levels in sseawater and oysters from the Delaware and Chesapeake Bays determined using several methods. Appl. Environ. Microbiol. 86: e01581-20.
    Pubmed PMC
  4. Cheng PKC, Wong DKK, Chung TWH, Lim WWL. 2005. Norovirus contamination found in oysters worldwide. J. Med. Virol. 76: 593-597.
    Pubmed
  5. Alfano-Sobsey E, Sweat D, Hall A, Breedlove F, Rodriguez R, Greene S, et al. 2012. Norovirus outbreak associated with undercooked oysters and secondary household transmission. Epidemiol. Infect. 140: 276-282.
    Pubmed
  6. Leclerc H, Schwartzbrod L, Dei-Cas E. 2002. Microbial agents associated with water-borne diseases. Crit. Rev. Microbiol. 28: 371-409.
    Pubmed
  7. Noble RT, Moore DF, Leecaster MK, McGee CD, Weisberg SB. 2003. Comparison of total coliform, fecal coliform, and enterococcus bacterial indicator response for ocean recreational water quality testing. Water Res. 37: 1637-1643.
    Pubmed
  8. Bower PA, Scopel CO, Jensen ET, Depas MM, McLellan SL. 2005. Detection of genetic markers of fecal indicator bacteria in Lake Michigan and determination of their relationship to Escherichia coli densities using standard microbiological methods. Appl. Environ. Microbiol. 71: 8305-8313.
    Pubmed PMC
  9. Farnleitner AH, Ryzinska-Paier G, Reischer GH, Burtscher MM, Knetsch S, Kirschner AKT, et al. 2010. Escherichia coli and enterococci are sensitive and reliable indicators for human, livestock and wildlife faecal pollution in alpine mountainous water resources. J. Appl. Microbiol. 109: 1599-1608.
    Pubmed PMC
  10. Savichtcheva O, Okabe S. 2006. Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res. 40: 2463-2476.
    Pubmed
  11. Giglio OG, Caggiano G, Bagordo F, Barbuti G, Brigida S, Lugoli F, et al. 2017. Enteric viruses and fecal bacteria indicators to assess groundwater quality and suitability for irrigation. Int. J. Environ. Res. Public. Health 14: 558.
    Pubmed PMC
  12. Vinjé J, Oudejans SJG, Stewart JR, Sobsey MD, Long SC. 2004. Molecular detection and genotyping of male-specific coliphages by reverse transcription-PCR and reverse line blot hybridization. Appl. Environ. Microbiol. 70: 5996-6004.
    Pubmed PMC
  13. Lee JE, Lee H, Cho YH, Hur HG, Ko G. 2011. F+ RNA coliphage-based microbial source tracking in water resources of South Korea. Sci. Total Environ. 412-413: 127-131.
    Pubmed
  14. Rezaeinejad S, Vergara GG, Woo CH, Lim TT, Sobsey MD, Gin KY. 2014. Surveillance of enteric viruses and coliphages in a tropical urban catchment. Water Res. 58: 122-131.
    Pubmed
  15. Cho K, Lee C, Park S, Kim JH, Choi YS, Kim MS, et al. 2018. Use of coliphages to investigate norovirus contamination in a shellfish growing area in Republic of Korea. Environ. Sci. Pollut. Res. Int. 25: 30044-30055.
    Pubmed
  16. Liang Z, He Z, Zhou X, Powell CA, Yang Y, He LM, et al. 2013. Impact of mixed land-use practices on the microbial water quality in a subtropical coastal watershed. Sci. Total Environ. 449: 426-433.
    Pubmed
  17. Lee J, Park S, Lee C, Cho K, Jeong YS, Kim YM, et al. 2020. Male-spcific and somatic coliphage profiles from major aquaculture areas in Republic of Korea. Food Environ. Virol. 12: 240-249.
    Pubmed
  18. Pratt B, Chang H. 2012. Effects of land cover, topography, and built structure on seasonal water quality at multiple spatial scales. J. Hazard. Mater. 209-210: 48-58.
    Pubmed
  19. U.S. Environmental Protection Agency. 2001. Method 1602: male specific (F+ ) and somatic coliphage in water by single agar layer (SAL) procedure. Washington, DC, USA: Office of Water, USEPA.
  20. Ko HY, Cho K, Park S, Kim JH, Kang JH, Jeong YS, et al. 2018. Host-specific Bacteroides markers-based microbial source tracking in aquaculture areas. Microbes Environ. 33: 151-161.
    Pubmed PMC
  21. Ministry of Environment, Republic of Korea. 2023. Official testing method with respect to water pollution process. Incheon, Republic of Korea: National Institute of Environmental Research.
  22. R Core Team. 2021. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from https://www.R-project.org. Accessed Sep. 25, 2024.
  23. Shanks OC, Nietch C, Simonich M, Younger M, Reynolds D, Field KG. 2005. Basin-wide analysis of the dynamics of fecal contamination and fecal source identification in Tillamook Bay, Oregon. Appl. Environ. Microbiol. 72: 5537-5546.
    Pubmed PMC
  24. Stea EC, Hansen LT, Jamieson RC, Yost CK. 2015. Fecal contamination in the surface waters of a rural- and an urban-source watershed. J. Environ. Qual. 44: 1556-1567.
    Pubmed
  25. Lipp EK, Kurz R, Vincent R, Rodriguez-Palacios C, Farrah SR, Rose JB. 2001. The effects of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary. Estuaries Coast 24: 266-276.
  26. Jofre J. 2007. Indicators of waterborne enteric viruses. Perspectives Med. Virol. 17: 227-249.
  27. Bertrand I, Schijven JF, Sanchez G, Wyn-Jones P, Ottoson J, Morin T, et al. 2012. The impact of temperature on the inactivation of enteric viruses in food and water: a review. J. Appl. Microbiol. 112: 1059-1074.
    Pubmed
  28. Wetz JJ, Lipp EK, Griffin DW, Lukasik J, Wait D, Sobsey MD, et al. 2004. Presence, infectivity, and stability of enteric viruses in seawater: relationship to marine water quality in the Florida Keys. Mar. Pollut. Bull. 48: 698-704.
    Pubmed
  29. Guibai L, Gregory J. 1991. Flocculation and sedimentation of high-turbidity waters. Water Res. 35: 1137-1143.
  30. McMinn BR, Huff EM, Rhodes ER, Korajkic A. 2017. Concentration and quantification of somatic and F+ coliphages from recreational waters. J. Virol. Methods 249: 58-65.
    Pubmed PMC

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Article

Research article

J. Microbiol. Biotechnol. 2024; 34(11): 2223-2230

Published online November 28, 2024 https://doi.org/10.4014/jmb.2406.06001

Copyright © The Korean Society for Microbiology and Biotechnology.

Distributions of Fecal Indicators at Aquaculture Areas in a Bay of Republic of Korea

SungJun Park1,2, Cheonghoon Lee1,3*, Sung Jae Jang1, Kyuseon Cho1, Jin Hwi Kim4, Woon-Ki Kim1,3, Joo-Hyon Kang5, Kwon-Sam Park6, and GwangPyo Ko1,2,3*

1Department of Environmental Health Sciences, Graduate School of Public Health, Seoul National University, Seoul 08826, Republic of Korea
2N-Bio, Seoul National University, Seoul 08826, Republic of Korea
3Institute of Health and Environment, Seoul National University, Seoul 08826, Republic of Korea
4Department of Civil and Environmental Engineering, Konkuk University-Seoul, Seoul 05029, Republic of Korea
5Department of Civil and Environmental Engineering, Dongguk University, Seoul 04620, Republic of Korea
6Department of Food Science and Biotechnology, Kunsan National University, Gunsan 54150, Republic of Korea

Correspondence to:Cheonghoon Lee,       shota2@snu.ac.kr
GwangPyo Ko,           gko@snu.ac.kr

Received: June 2, 2024; Revised: September 27, 2024; Accepted: October 2, 2024

Abstract

Aquaculture products, such as clams, scallops, and oysters, are major vectors of fecal-derived pathogens. Male-specific and somatic coliphages are strongly correlated with human noroviruses, the major enteric viruses worldwide. Geographic information system with local land-use patterns can also provide valuable information for tracking sources of fecal-derived pathogens. We examined distributions of four fecal indicator microorganisms, i.e., male-specific and somatic coliphage, total coliform, and Escherichia coli (E. coli) in three river and seawater sampling sites located on the coast of Gomso Bay in the Republic of Korea during the sampling period (from March 2015 to January 2016). Geospatial analyses of fecal indicators and correlations between environmental parameters and fecal indicators or among fecal indicators were also performed. Overall, river water samples showed highest concentrations of both types of coliphage in summer (July 2015). High concentrations of both total coliform and E. coli were detected in river water during the period from July to September 2015. High concentrations of all fecal indicators were found at site GL02, located in the innermost part of Gomso Bay, which has high-density agriculture and residential areas. Environmental factors related to precipitation—cumulative precipitation on and from 3 days before the sampling day (Prep-0 and Prep-3, respectively)—and salinity were strongly correlated with the concentrations of all fecal indicators. The present results suggest that investigations of multiple fecal indicators with systemic geospatial information are necessary for precisely tracking fecal contaminations of aquaculture products.

Keywords: Fecal contamination, fecal indicator, geographical information system, male-specific coliphage, microbial source tracking, somatic coliphage

References

  1. Iritani N, Kaida A, Abe N, Kubo H, Sekiguchi JI, Yamamoto SP, et al. 2014. Detection and genetic characterization of human enteric viruses in oyster-associated gastroenteritis outbreaks between 2001 and 2012 in Osaka city, Japan. J. Med. Virol. 86: 2019-2025.
    Pubmed
  2. Sutthikornchai C, Popruk S, Chumpolbanchorn K, Sukhumavasi W, Sukthana Y. 2016. Oyster is an effective transmission vehicle for Cryptosporidium infection in human. Asian Pac. J. Trop. Med. 9: 562-566.
    Pubmed
  3. Parveen S, Jacobs J, Ozbay G, Chintapenta LK, Almuhaideb E, Meredith J, et al. 2020. Seasonal and geographical differences in total and pathogenic Vibrio parahaemolyticus and Vibrio vulnificus levels in sseawater and oysters from the Delaware and Chesapeake Bays determined using several methods. Appl. Environ. Microbiol. 86: e01581-20.
    Pubmed KoreaMed
  4. Cheng PKC, Wong DKK, Chung TWH, Lim WWL. 2005. Norovirus contamination found in oysters worldwide. J. Med. Virol. 76: 593-597.
    Pubmed
  5. Alfano-Sobsey E, Sweat D, Hall A, Breedlove F, Rodriguez R, Greene S, et al. 2012. Norovirus outbreak associated with undercooked oysters and secondary household transmission. Epidemiol. Infect. 140: 276-282.
    Pubmed
  6. Leclerc H, Schwartzbrod L, Dei-Cas E. 2002. Microbial agents associated with water-borne diseases. Crit. Rev. Microbiol. 28: 371-409.
    Pubmed
  7. Noble RT, Moore DF, Leecaster MK, McGee CD, Weisberg SB. 2003. Comparison of total coliform, fecal coliform, and enterococcus bacterial indicator response for ocean recreational water quality testing. Water Res. 37: 1637-1643.
    Pubmed
  8. Bower PA, Scopel CO, Jensen ET, Depas MM, McLellan SL. 2005. Detection of genetic markers of fecal indicator bacteria in Lake Michigan and determination of their relationship to Escherichia coli densities using standard microbiological methods. Appl. Environ. Microbiol. 71: 8305-8313.
    Pubmed KoreaMed
  9. Farnleitner AH, Ryzinska-Paier G, Reischer GH, Burtscher MM, Knetsch S, Kirschner AKT, et al. 2010. Escherichia coli and enterococci are sensitive and reliable indicators for human, livestock and wildlife faecal pollution in alpine mountainous water resources. J. Appl. Microbiol. 109: 1599-1608.
    Pubmed KoreaMed
  10. Savichtcheva O, Okabe S. 2006. Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res. 40: 2463-2476.
    Pubmed
  11. Giglio OG, Caggiano G, Bagordo F, Barbuti G, Brigida S, Lugoli F, et al. 2017. Enteric viruses and fecal bacteria indicators to assess groundwater quality and suitability for irrigation. Int. J. Environ. Res. Public. Health 14: 558.
    Pubmed KoreaMed
  12. Vinjé J, Oudejans SJG, Stewart JR, Sobsey MD, Long SC. 2004. Molecular detection and genotyping of male-specific coliphages by reverse transcription-PCR and reverse line blot hybridization. Appl. Environ. Microbiol. 70: 5996-6004.
    Pubmed KoreaMed
  13. Lee JE, Lee H, Cho YH, Hur HG, Ko G. 2011. F+ RNA coliphage-based microbial source tracking in water resources of South Korea. Sci. Total Environ. 412-413: 127-131.
    Pubmed
  14. Rezaeinejad S, Vergara GG, Woo CH, Lim TT, Sobsey MD, Gin KY. 2014. Surveillance of enteric viruses and coliphages in a tropical urban catchment. Water Res. 58: 122-131.
    Pubmed
  15. Cho K, Lee C, Park S, Kim JH, Choi YS, Kim MS, et al. 2018. Use of coliphages to investigate norovirus contamination in a shellfish growing area in Republic of Korea. Environ. Sci. Pollut. Res. Int. 25: 30044-30055.
    Pubmed
  16. Liang Z, He Z, Zhou X, Powell CA, Yang Y, He LM, et al. 2013. Impact of mixed land-use practices on the microbial water quality in a subtropical coastal watershed. Sci. Total Environ. 449: 426-433.
    Pubmed
  17. Lee J, Park S, Lee C, Cho K, Jeong YS, Kim YM, et al. 2020. Male-spcific and somatic coliphage profiles from major aquaculture areas in Republic of Korea. Food Environ. Virol. 12: 240-249.
    Pubmed
  18. Pratt B, Chang H. 2012. Effects of land cover, topography, and built structure on seasonal water quality at multiple spatial scales. J. Hazard. Mater. 209-210: 48-58.
    Pubmed
  19. U.S. Environmental Protection Agency. 2001. Method 1602: male specific (F+ ) and somatic coliphage in water by single agar layer (SAL) procedure. Washington, DC, USA: Office of Water, USEPA.
  20. Ko HY, Cho K, Park S, Kim JH, Kang JH, Jeong YS, et al. 2018. Host-specific Bacteroides markers-based microbial source tracking in aquaculture areas. Microbes Environ. 33: 151-161.
    Pubmed KoreaMed
  21. Ministry of Environment, Republic of Korea. 2023. Official testing method with respect to water pollution process. Incheon, Republic of Korea: National Institute of Environmental Research.
  22. R Core Team. 2021. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from https://www.R-project.org. Accessed Sep. 25, 2024.
  23. Shanks OC, Nietch C, Simonich M, Younger M, Reynolds D, Field KG. 2005. Basin-wide analysis of the dynamics of fecal contamination and fecal source identification in Tillamook Bay, Oregon. Appl. Environ. Microbiol. 72: 5537-5546.
    Pubmed KoreaMed
  24. Stea EC, Hansen LT, Jamieson RC, Yost CK. 2015. Fecal contamination in the surface waters of a rural- and an urban-source watershed. J. Environ. Qual. 44: 1556-1567.
    Pubmed
  25. Lipp EK, Kurz R, Vincent R, Rodriguez-Palacios C, Farrah SR, Rose JB. 2001. The effects of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary. Estuaries Coast 24: 266-276.
  26. Jofre J. 2007. Indicators of waterborne enteric viruses. Perspectives Med. Virol. 17: 227-249.
  27. Bertrand I, Schijven JF, Sanchez G, Wyn-Jones P, Ottoson J, Morin T, et al. 2012. The impact of temperature on the inactivation of enteric viruses in food and water: a review. J. Appl. Microbiol. 112: 1059-1074.
    Pubmed
  28. Wetz JJ, Lipp EK, Griffin DW, Lukasik J, Wait D, Sobsey MD, et al. 2004. Presence, infectivity, and stability of enteric viruses in seawater: relationship to marine water quality in the Florida Keys. Mar. Pollut. Bull. 48: 698-704.
    Pubmed
  29. Guibai L, Gregory J. 1991. Flocculation and sedimentation of high-turbidity waters. Water Res. 35: 1137-1143.
  30. McMinn BR, Huff EM, Rhodes ER, Korajkic A. 2017. Concentration and quantification of somatic and F+ coliphages from recreational waters. J. Virol. Methods 249: 58-65.
    Pubmed KoreaMed