Persistence of Bacteroides ovatus under simulated sunlight irradiation

BMC Microbiology

Thanh H Nguyen²  Pei-Ying Hong¹  Shengkun Dong² 

[1] Water Desalination and Reuse Center, Environmental Science and Engineering Program, King Abdullah University of Science and Technology (KAUST), 4700 King Abdullah Boulevard, Thuwal 23955-6900, Saudi Arabia;Department of Civil and Environmental Engineering, University of Illinois at Urbana-Champaign, 205 N. Mathews, 3230 Newmark Lab, Urbana, IL 61801, USA

关键词: PMA-qPCR;    Freshwater;    Seawater;    Fate and persistence;    Sunlight irradiation;    Bacteroides ovatus;   

Others  :  1140851
DOI  :  10.1186/1471-2180-14-178

 received in 2014-01-01, accepted in 2014-06-26,  发布年份 2014

【 摘 要 】

Background

Bacteroides ovatus, a member of the genus Bacteroides, is considered for use in molecular-based methods as a general fecal indicator. However, knowledge on its fate and persistence after a fecal contamination event remains limited. In this study, the persistence of B. ovatus was evaluated under simulated sunlight exposure and in conditions similar to freshwater and seawater. By combining propidium monoazide (PMA) treatment and quantitative polymerase chain reaction (qPCR) detection, the decay rates of B. ovatus were determined in the presence and absence of exogenous photosensitizers and in salinity up to 39.5 parts per thousand at 27°C.

Results

UVB was found to be important for B. ovatus decay, averaging a 4 log₁₀ of decay over 6 h of exposure without the presence of extracellular photosensitizers. The addition of NaNO₂, an exogenous sensitizer producing hydroxyl radicals, did not significantly change the decay rate of B. ovatus in both low and high salinity water, while the exogenous sensitizer algae organic matter (AOM) slowed down the decay of B. ovatus in low salinity water. At seawater salinity, the decay rate of B. ovatus was slower than that in low salinity water, except when both NaNO₂ and AOM were present.

Conclusion

The results of laboratory experiments suggest that if B. ovatus is released into either freshwater or seawater environment in the evening, 50% of it may be intact by the next morning; if it is released at noon, only 50% may be intact after a mere 5 min of full spectrum irradiation on a clear day. This study provides a mechanistic understanding to some of the important environmental relevant factors that influenced the inactivation kinetics of B. ovatus in the presence of sunlight irradiation, and would facilitate the use of B. ovatus to indicate the occurrence of fecal contamination.

【 授权许可】

   
2014 Dong et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

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【 参考文献 】

• [1]Cabelli VJ, Dufour AP, McCabe LJ, Levin MA: A marine recreational water quality criterion consistent with indicator concepts and risk analysis. J Water Pollut Control Fed 1983, 55(10):1306-1314.
• [2]Stevenson AH: Studies of bathing water quality and health. Am J Public Health Nations Health 1953, 43(5 Pt 1):529-538.
• [3]Menon P, Billen G, Servais P: Mortality rates of autochthonous and fecal bacteria in natural aquatic ecosystems. Water Res 2003, 37(17):4151-4158.
• [4]Bae S, Wuertz S: Discrimination of viable and dead fecal Bacteroidales bacteria by quantitative PCR with propidium monoazide. Appl Environ Microbiol 2009, 75(9):2940-2944.
• [5]Hou D, Rabinovici SJM, Boehm AB: Enterococci predictions from partial least squares regression models in conjunction with a single-sample standard improve the efficacy of beach management advisories. Environ Sci Technol 2006, 40(6):1737-1743.
• [6]Bae S, Wuertz S: Rapid decay of host-specific fecal Bacteroidales cells in seawater as measured by quantitative PCR with propidium monoazide. Water Res 2009, 43(19):4850-4859.
• [7]Fiksdal L, Maki JS, LaCroix SJ, Staley JT: Survival and detection of Bacteroides spp., prospective indicator bacteria. Appl Environ Microbiol 1985, 49(1):148-150.
• [8]Shanks OC, White K, Kelty CA, Hayes S, Sivaganesan M, Jenkins M, Varma M, Haugland RA: Performance assessment PCR-based assays targeting bacteroidales genetic markers of bovine fecal pollution. Appl Environ Microbiol 2010, 76(5):1359-1366.
• [9]Hong P-Y, Wu J-H, Liu W-T: A high-throughput and quantitative hierarchical oligonucleotide primer extension (HOPE)-based approach to identify sources of faecal contamination in water bodies. Environ Microbiol 2009, 11(7):1672-1681.
• [10]Bernhard AE, Field KG: Identification of nonpoint sources of fecal pollution in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes. Appl Environ Microbiol 2000, 66(4):1587-1594.
• [11]Whitman RL, Nevers MB, Korinek GC, Byappanahalli MN: Solar and temporal effects on Escherichia coli concentration at a lake Michigan swimming beach. Appl Environ Microbiol 2004, 70(7):4276-4285.
• [12]Ubomba-Jaswa E, Fernandez-Ibanez P, Navntoft C, Polo-Lopez MI, McGuigan KG: Investigating the microbial inactivation efficiency of a 25 L batch solar disinfection (SODIS) reactor enhanced with a compound parabolic collector (CPC) for household use. J Chem Technol Biotechnol 2010, 85(8):1028-1037.
• [13]Sinton L, Hall C, Braithwaite R: Sunlight inactivation of Campylobacter jejuni and Salmonella enterica, compared with Escherichia coli, in seawater and river water. J Water Health 2007, 5(3):357-365.
• [14]Walters SP, Yamahara KM, Boehm AB: Persistence of nucleic acid markers of health-relevant organisms in seawater microcosms: implications for their use in assessing risk in recreational waters. Water Res 2009, 43(19):4929-4939.
• [15]Okabe S, Shimazu Y: Persistence of host-specific Bacteroides–Prevotella 16S rRNA genetic markers in environmental waters: effects of temperature and salinity. Appl Microbiol Biotechnol 2007, 76(4):935-944.
• [16]Bell A, Layton AC, McKay L, Williams D, Gentry R, Sayler GS: Factors influencing the persistence of fecal Bacteroides in stream water. J Environ Qual 2009, 38(3):1224-1232.
• [17]Bae S, Wuertz S: Survival of host-associated Bacteroidales cells and their relationship with Enterococcus spp., Campylobacter jejuni, Salmonella enterica Serovar Typhimurium, and adenovirus in freshwater microcosms as measured by propidium monoazide-quantitative PCR. Appl Environ Microbiol 2012, 78(4):922-932.
• [18]Davies-Colley RJ, Donnison AM, Speed DJ, Ross CM, Nagels JW: Inactivation of faecal indicator micro-organisms in waste stabilisation ponds: interactions of environmental factors with sunlight. Water Res 1999, 33(5):1220-1230.
• [19]Boehm AB, Yamahara KM, Love DC, Peterson BM, McNeill K, Nelson KL: Covariation and photoinactivation of traditional and novel indicator organisms and human viruses at a sewage-impacted marine beach. Environ Sci Technol 2009, 43(21):8046-8052.
• [20]Santos AL, Gomes NCM, Henriques I, Almeida A, Correia A, Cunha A: Contribution of reactive oxygen species to UV-B-induced damage in bacteria. J Photochem Photobiol B 2012, 117:40-46.
• [21]van der Meulen FW, Ibrahim K, Sterenborg HJ, Alphen LV, Maikoe A, Dankert J: Photodynamic destruction of Haemophilus parainfluenzae by endogenously produced porphyrins. J Photochem Photobiol B 1997, 40(3):204-208.
• [22]He YY, Hader DP: Involvement of reactive oxygen species in the UV-B damage to the cyanobacterium Anabaena sp. J Photochem Photobiol B 2002, 66(1):73-80.
• [23]Romero-Maraccini OC, Sadik NJ, Rosado-Lausell SL, Pugh CR, Niu X-Z, Croué J-P, Nguyen TH: Sunlight-induced inactivation of human Wa and porcine OSU rotaviruses in the presence of exogenous photosensitizers. Environ Sci Technol 2013, 47(19):11004-11012.
• [24]Silverman AI, Peterson BM, Boehm AB, McNeill K, Nelson KL: Sunlight inactivation of human viruses and bacteriophages in coastal waters containing natural photosensitizers. Environ Sci Technol 2013, 47(4):1870-1878.
• [25]Maraccini PA, Ferguson DM, Boehm AB: Diurnal variation in Enterococcus species composition in polluted ocean water and a potential role for the enterococcal carotenoid in protection against photoinactivation. Appl Environ Microbiol 2012, 78(2):305-310.
• [26]Horner RA: A Taxonomic Guide to Some Common Marine Phytoplankton. UK: Biopress; 2002.
• [27]Robert C, Bernalier-Donadille A: The cellulolytic microflora of the human colon: evidence of microcrystalline cellulose-degrading bacteria in methane-excreting subjects. FEMS Microbiol Ecol 2003, 46(1):81-89.
• [28]Francis L, Ghaffour N, Alsaadi AS, Nunes SP, Amy GL: Performance evaluation of the DCMD desalination process under bench scale and large scale module operating conditions. J Membr Sci 2014, 455:103-112.
• [29]Romero OC, Straub AP, Kohn T, Nguyen TH: Role of temperature and suwannee river natural organic matter on inactivation kinetics of rotavirus and bacteriophage MS2 by solar irradiation. Environ Sci Technol 2011, 45(24):10385-10393.
• [30]Rojanasakul Y, Wang L, Hoffman AH, Shi X, Dalal NS, Banks DE, Ma JK: Mechanisms of hydroxyl free radical-induced cellular injury and calcium overloading in alveolar macrophages. Am J Respir Cell Mol Biol 1993, 8(4):377-383.
• [31]Carlsson J, Wrethen J, Beckman G: Superoxide dismutase in Bacteroides fragilis and related Bacteroides species. J Clin Microbiol 1977, 6(3):280-284.
• [32]Gregory EM, Moore WE, Holdeman LV: Superoxide dismutase in anaerobes: survey. Appl Environ Microbiol 1978, 35(5):988-991.
• [33]Eischeid AC, Linden KG: Molecular indications of protein damage in adenoviruses after UV disinfection. Appl Environ Microbiol 2011, 77(3):1145-1147.
• [34]Tuveson RW, Larson RA, Kagan J: Role of cloned carotenoid genes expressed in Escherichia coli in protecting against inactivation by near-UV light and specific phototoxic molecules. J Bacteriol 1988, 170(10):4675-4680.
• [35]McKinney CW, Pruden A: Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ Sci Technol 2012, 46(24):13393-13400.
• [36]Eddy FB, Williams E: Nitrite and freshwater fish. Chem Ecol 1987, 3(1):1-38.
• [37]Garside C: A chemiluminescent technique for the determination of nanomolar concentrations of nitrate and nitrite in seawater. Mar Chem 1982, 11(2):159-167.
• [38]Rubio D, Nebot E, Casanueva JF, Pulgarin C: Comparative effect of simulated solar light, UV, UV/H202 and photo-Fenton treatment (UV Vis/H2O2/Fe-2+, Fe-3+) in the Escherichia colt inactivation in artificial seawater. Water Res 2013, 47(16):6367-6379.
• [39]Wyer MD, Kay D, Watkins J, Davies C, Kay C, Thomas R, Porter J, Stapleton CM, Moore H: Evaluating short-term changes in recreational water quality during a hydrograph event using a combination of microbial tracers, environmental microbiology, microbial source tracking and hydrological techniques: a case study in Southwest Wales, UK. Water Res 2010, 44(16):4783-4795.
• [40]Stapleton CM, Kay D, Wyer MD, Davies C, Watkins J, Kay C, McDonald AT, Porter J, Gawler A: Evaluating the operational utility of a Bacteroidales quantitative PCR-based MST approach in determining the source of faecal indicator organisms at a UK bathing water. Water Res 2009, 43(19):4888-4899.