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Importance of Local and Regional Scales in Shaping Mycobacterial Abundance in Freshwater Lakes

  • Microbiology of Aquatic Systems
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Abstract

Biogeographical studies considering the entire bacterial community may underestimate mechanisms of bacterial assemblages at lower taxonomic levels. In this context, the study aimed to identify factors affecting the spatial and temporal dynamic of the Mycobacterium, a genus widespread in aquatic ecosystems. Nontuberculous mycobacteria (NTM) density variations were quantified in the water column of freshwater lakes at the regional scale (annual monitoring of 49 lakes in the Paris area) and at the local scale (2-year monthly monitoring in Créteil Lake) by real-time quantitative PCR targeting the atpE gene. At the regional scale, mycobacteria densities in water samples ranged from 6.7 × 103 to 1.9 × 108 genome units per liter. Density variations were primarily explained by water pH, labile iron, and dispersal processes through the connection of the lakes to a river. In Créteil Lake, no spatial variation of mycobacterial densities was noticed over the 2-year monthly survey, except after large rainfall events. Indeed, storm sewer effluents locally and temporarily increased NTM densities in the water column. The temporal dynamic of the NTM densities in Créteil Lake was associated with suspended solid concentrations. No clear seasonal variation was noticed despite a shift in NTM densities observed over the 2012–2013 winter. Temporal NTM densities fluctuations were well predicted by the neutral community model, suggesting a random balance between loss and gain of mycobacterial taxa within Créteil Lake. This study highlights the importance of considering multiple spatial scales for understanding the spatio-temporal dynamic of bacterial populations in natural environments.

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References

  1. Hruska K, Kaevska M (2012) Mycobacteria in water, soil, plants and air: a review. Vet Med (Praha) 57:623–679

    Article  Google Scholar 

  2. Seo J-S, Keum Y-S, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6:278–309. https://doi.org/10.3390/ijerph6010278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Falkinham III JO (1996) Epidemiology of infection by nontuberculous mycobacteria. Clin Microbiol Rev 9:177–215

    PubMed  PubMed Central  Google Scholar 

  4. Mrlik V, Slany M, Kubecka J, et al. (2012) A low prevalence of mycobacteria in freshwater fish from water reservoirs, ponds and farms. J Fish Dis 35:497–504. https://doi.org/10.1111/j.1365-2761.2012.01369.x

    Article  CAS  PubMed  Google Scholar 

  5. Prevots DR, Marras TK (2015) Epidemiology of human pulmonary infection with nontuberculous mycobacteria a review. Clin Chest Med 36:13–34. https://doi.org/10.1016/j.ccm.2014.10.002

    Article  PubMed  Google Scholar 

  6. Covert TC, Rodgers MR, Reyes AL, Stelma GN (1999) Occurrence of nontuberculous mycobacteria in environmental samples. Appl Environ Microbiol 65:2492–2496

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Falkinham III JO, Norton CD, LeChevalier MW (2001) Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other mycobacteria in drinking water distribution systems. Appl Environ Microbiol 67:1225–1231. https://doi.org/10.1128/AEM.67.3.1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Vaerewijck MJM, Huys G, Palomino JC, et al. (2005) Mycobacteria in drinking water distribution systems: ecology and significance for human health. FEMS Microbiol Rev 29:911–934. https://doi.org/10.1016/j.femsre.2005.02.001

    Article  CAS  PubMed  Google Scholar 

  9. du Moulin G, Stottmeier K, Pelletier P, et al. (1988) Concentration of Mycobacterium avium by hospital hot water systems. JAMA 260:1599–1601

    Article  PubMed  Google Scholar 

  10. Fox GE, Wisotzkey JD, Jurtshuk P (1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170. https://doi.org/10.1099/00207713-42-1-166

    Article  CAS  PubMed  Google Scholar 

  11. Fujita J, Nanki N, Negayama K, et al. (2002) Nosocomial contamination by Mycobacterium gordonae in hospital water supply and super-oxidized water. J Hosp Infect 51:65–68. https://doi.org/10.1053/jhin.2002.1197

    Article  PubMed  Google Scholar 

  12. Niva M, Hernesmaa A, Haahtela K, et al. (2006) Actinobacterial communities of boreal forest soil and lake water are rich in mycobacteria. Boreal Environ Res 11:45–53

    Google Scholar 

  13. Roguet A, Therial C, Saad M, et al. (2016) High mycobacterial diversity in recreational lakes. Antonie Van Leeuwenhoek 109:1–13. https://doi.org/10.1007/s10482-016-0665-x

    Article  Google Scholar 

  14. Khera T (2012) The diversity and distribution of Mycobacterium species in varying ecological and climatic environments. Doctoral dissertation, University of Warwick

  15. Lee CS, Kim M, Lee C, et al. (2016) The microbiota of recreational freshwaters and the implications for environmental and public health. Front Microbiol 7:1826. https://doi.org/10.3389/fmicb.2016.01826

    PubMed  PubMed Central  Google Scholar 

  16. Unno T, Kim J, Kim Y, et al. (2015) Influence of seawater intrusion on microbial communities in groundwater. Sci Total Environ 532:337–343. https://doi.org/10.1016/j.scitotenv.2015.05.111

    Article  CAS  PubMed  Google Scholar 

  17. Falkinham III JO (2002) Nontuberculous mycobacteria in the environment. Clin Chest Med 23:529–551

    Article  PubMed  Google Scholar 

  18. Amaro A, Duarte E, Amado A, et al. (2008) Comparison of three DNA extraction methods for Mycobacterium bovis, Mycobacterium tuberculosis and Mycobacterium avium subsp. avium. Lett Appl Microbiol 47:8–11. https://doi.org/10.1111/j.1472-765X.2008.02372.x

    Article  CAS  PubMed  Google Scholar 

  19. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206. https://doi.org/10.1086/652373

    Article  PubMed  Google Scholar 

  20. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:1–10. https://doi.org/10.1038/nrmicro2795

    Article  Google Scholar 

  21. Leibold MA, Holyoak M, Mouquet N, et al. (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. https://doi.org/10.1111/j.1461-0248.2004.00608.x

    Article  Google Scholar 

  22. Martiny JBH, Bohannan BJM, Brown JH, et al. (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. https://doi.org/10.1038/nrmicro1341

    Article  CAS  PubMed  Google Scholar 

  23. Östman Ö, Drakare S, Kritzberg ES, et al. (2010) Regional invariance among microbial communities. Ecol Lett 13:118–127. https://doi.org/10.1111/j.1461-0248.2009.01413.x

    Article  PubMed  Google Scholar 

  24. Roguet A, Laigle GS, Therial C, et al. (2015) Neutral community model explains the bacterial community assembly in freshwater lakes. FEMS Microbiol Ecol 91:1–11. https://doi.org/10.1093/femsec/fiv125

    Article  Google Scholar 

  25. Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227. https://doi.org/10.1038/35012228

    Article  CAS  PubMed  Google Scholar 

  26. Ilmonen J, Paasivirta L, Virtanen R, Muotka T (2009) Regional and local drivers of macroinvertebrate assemblages in boreal springs. J Biogeogr 36:822–834. https://doi.org/10.1111/j.1365-2699.2008.02045.x

    Article  Google Scholar 

  27. Viallier J, Viallier G (1973) Inventaire des mycobacteries de la nature. Ann Soc Belg Med Trop (1920) 53:361–371

    CAS  Google Scholar 

  28. Stinear T, Davies JK, Jenkin GA, et al. (2000) Identification of Mycobacterium ulcerans in the environment from regions in Southeast Australia in which it is endemic with sequence capture-PCR. Appl Environ Microbiol 66:3206–3213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Pickup RW, Rhodes G, Arnott S, et al. (2005) Mycobacterium avium subsp. paratuberculosis in the catchment area and water of the River Taff in South Wales, United Kingdom, and its potential relationship to clustering of Crohn’s disease cases in the city of Cardiff. Appl Environ Microbiol 71:2130–2139. https://doi.org/10.1128/AEM.71.4.2130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Pickup RW, Rhodes G, Bull TJ, et al. (2006) Mycobacterium avium subsp. paratuberculosis in lake catchments, in river water abstracted for domestic use, and in effluent from domestic sewage treatment works: diverse opportunities for environmental cycling and human exposure. Appl Environ Microbiol 72:4067–4077. https://doi.org/10.1128/AEM.02490-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gauthier DT, Reece KS, Xiao J, et al. (2010) Quantitative PCR assay for Mycobacterium pseudoshottsii and Mycobacterium shottsii and application to environmental samples and fishes from the Chesapeake Bay. Appl Environ Microbiol 76:6171–6179. https://doi.org/10.1128/AEM.01091-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bland CS, Ireland JM, Lozano E, et al. (2005) Mycobacterial ecology of the Rio Grande. Appl Environ Microbiol 71:5719–5727. https://doi.org/10.1128/AEM.71.10.5719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rahbar M, Lamei A, Babazadeh H, Yavari SA (2010) Isolation of rapid growing mycobacteria from soil and water in Iran. Afr J Biotechnol 9:3618–3621

    Google Scholar 

  34. Kirschner RA, Parker BC, Falkinham III JO (1999) Humic and fulvic acids stimulate the growth of Mycobacterium avium. FEMS Microbiol Ecol 30:327–332

    Article  CAS  PubMed  Google Scholar 

  35. Iivanainen EK, Martikainen PJ, Väänänen PK, Katila ML (1993) Environmental factors affecting the occurrence of mycobacteria in brook waters. Appl Environ Microbiol 59:398–404

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Catherine A, Troussellier M, Bernard C (2008) Design and application of a stratified sampling strategy to study the regional distribution of cyanobacteria (Ile-de-France, France). Water Res 42:4989–5001. https://doi.org/10.1016/j.watres.2008.09.028

    Article  CAS  PubMed  Google Scholar 

  37. Catherine A, Mouillot D, Escoffier N, et al. (2010) Cost effective prediction of the eutrophication status of lakes and reservoirs. Freshw Biol 55:2425–2435. https://doi.org/10.1111/j.1365-2427.2010.02452.x

    Article  Google Scholar 

  38. Radomski N, Roguet A, Lucas FS, et al. (2013) atpE gene as a new useful specific molecular target to quantify Mycobacterium in environmental samples. BMC Microbiol 13:277. https://doi.org/10.1186/1471-2180-13-277

    Article  PubMed  PubMed Central  Google Scholar 

  39. Wurtzer S, Prevost B, Lucas FS, Moulin L (2014) Detection of enterovirus in environmental waters: a new optimized method compared to commercial real-time RT-qPCR kits. J Virol Methods 209:47–54. https://doi.org/10.1016/j.jviromet.2014.08.016

    Article  CAS  PubMed  Google Scholar 

  40. Rogora M, Minella M, Orrù A, Tartari GA (2006) A comparison between high-temperature catalytic oxidation and persulphate oxidation for the determination of total nitrogen in freshwater. Int J Environ Anal Chem 86:1065–1078. https://doi.org/10.1080/03067310600739632

    Article  CAS  Google Scholar 

  41. Bressy A, Gromaire MC, Lorgeoux C, Chebbo G (2011) Alkylphenols in atmospheric depositions and urban runoff. Water Sci Technol 63(4):671–679. https://doi.org/10.2166/wst.2011.121

    Article  CAS  PubMed  Google Scholar 

  42. Chaminda GGT, Nakajima F, Furumai H (2008) Heavy metal (Zn and Cu) complexation and molecular size distribution in wastewater treatment plant effluent. Water Sci Technol 58:1207–1213

    Article  CAS  PubMed  Google Scholar 

  43. R Core Team (2016) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, http://www.R-project.org/

    Google Scholar 

  44. Kratzer CR, Brezonik PL (1981) A Carlson-type trophic state index for nitrogen in Florida lakes. Water Resour Bull Am Water Resour Assoc 17:713–715. https://doi.org/10.1111/j.1752-1688.1981.tb01282.x

    Article  CAS  Google Scholar 

  45. Carlson RE (1977) A trophic state index for lakes. Limnol Oceanogr 22:361–369. https://doi.org/10.4319/lo.1977.22.2.0361

    Article  CAS  Google Scholar 

  46. Rogerson PA (2001) Statistical methods for geography. Sage Publications, London,

    Book  Google Scholar 

  47. Zuur A, Ieno EN, Walker N, et al. (2009) Mixed effects models and extensions in ecology with R. Springer Science and Business Media, New-York,

    Book  Google Scholar 

  48. Pinheiro J, Bates D, DebRoy S, Sarkar D (2015) Package “nlme”. Fit and compare Gaussian linear and nonlinear mixed-effects models, version 3.1–120

  49. Ofiţeru ID, Lunn M, Curtis TP, et al. (2010) Combined niche and neutral effects in a microbial wastewater treatment community. Proc Natl Acad Sci USA 107:15345–15350. https://doi.org/10.1073/pnas.1000604107

    Article  PubMed  PubMed Central  Google Scholar 

  50. Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S (2015) Package “multcomp”. Simultaneous inference in general parametric models, version 1.4–0

  51. Radomski N, Cambau E, Moulin L, et al. (2010) Comparison of culture methods for isolation of nontuberculous mycobacteria from surface waters. Appl Environ Microbiol 76:3514–3520. https://doi.org/10.1128/AEM.02659-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Radomski N, Lucas FS, Moilleron R, et al. (2010) Development of a real-time qPCR method for detection and enumeration of Mycobacterium spp. in surface water. Appl Environ Microbiol 76:7348–7351. https://doi.org/10.1128/AEM.00942-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Josephon KL, Gerba CP, Pepper IL (1993) Polymerase chain reaction detection of nonviable. Appl Environ Microbiol 59:3513–3515

    Google Scholar 

  54. Masters CI, Shallcross JA, Mackey BM (1994) Effect of stress treatments on the detection of Listeria monocytogenes and enterotoxigenic Escherichia coli by the polymerase chain reaction. J Appl Bacteriol 77:73–79

    Article  CAS  PubMed  Google Scholar 

  55. Guo F, Zhang T (2013) Biases during DNA extraction of activated sludge samples revealed by high throughput sequencing. Appl Microbiol Biotechnol 97:4607–4616. https://doi.org/10.1007/s00253-012-4244-4

    Article  CAS  PubMed  Google Scholar 

  56. Jacobs J, Rhodes M, Sturgis B, Wood B (2009) Influence of environmental gradients on the abundance and distribution of Mycobacterium spp. in a coastal lagoon estuary. Appl Environ Microbiol 75:7378–7384. https://doi.org/10.1128/AEM.01900-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Slana I, Kralik P, Kralova A, Pavlik I (2008) On-farm spread of Mycobacterium avium subsp. paratuberculosis in raw milk studied by IS900 and F57 competitive real time quantitative PCR and culture examination. Int J Food Microbiol 128:250–257. https://doi.org/10.1016/j.ijfoodmicro.2008.08.013

    Article  CAS  PubMed  Google Scholar 

  58. Radomski N (2011) Sources of nontuberculous mycobacteria in watersheds. Doctoral dissertation, Université Paris-Est École des Ponts ParisTech

  59. Lindström ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep 4:1–9. https://doi.org/10.1111/j.1758-2229.2011.00257.x

    Article  PubMed  Google Scholar 

  60. Norby B, Fosgate GT, Manning EJB, et al. (2007) Environmental mycobacteria in soil and water on beef ranches: association between presence of cultivable mycobacteria and soil and water physicochemical characteristics. Vet Microbiol 124:153–159. https://doi.org/10.1016/j.vetmic.2007.04.015

    Article  CAS  PubMed  Google Scholar 

  61. Mckay RML, Bullerjahn GS, Porta D, et al. (2004) Consideration of the bioavailability of iron in the north American Great Lakes: development of novel approaches toward understanding iron biogeochemistry. Aquat Ecosyst Heal Manag 7:475–490. https://doi.org/10.1080/14634980490513364

    Article  CAS  Google Scholar 

  62. Barclay R, Ratledge C (1983) Iron-binding compounds of Mycobacterium avium, M. intracellulare, M. scrofulaceum, and mycobactin-dependent M. paratuberculosis and M. avium. J Bacteriol 153:1138–1146

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Chan K (2009) Exochelin production in Mycobacterium neoaurum. Int. J. Mol. Sci. 10:345–353. https://doi.org/10.3390/ijms10010345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Emmenegger L, Sigg L, Sulzberger B (2001) Light-induced redox cycling of iron in circumneutral lakes. Limnol Oceanogr 46:49–61

    Article  CAS  Google Scholar 

  65. Uyttebroek M, Breugelmans P, Janssen M, et al. (2006) Distribution of the Mycobacterium community and polycyclic aromatic hydrocarbons (PAHs) among different size fractions of a long-term PAH-contaminated soil. Environ Microbiol 8:836–847. https://doi.org/10.1111/j.1462-2920.2005.00970.x

    Article  CAS  PubMed  Google Scholar 

  66. Uyttebroek M, Spoden A, Ortega-Calvo J-J, et al. (2007) Differential responses of eubacterial, Mycobacterium, and Sphingomonas communities in polycyclic aromatic hydrocarbon (PAH)-contaminated soil to artificially induced changes in PAH profile. Appl Environ Microbiol 36:1403–1411. https://doi.org/10.2134/jeq2006.0471

    CAS  Google Scholar 

  67. Debruyn JM, Mead TJ, Wilhelm SW, Sayler GS (2009) PAH biodegradative genotypes in Lake Erie sediments: evidence for broad geographical distribution of pyrene-degrading mycobacteria. Environ Sci Technol 43:3467–3473

    Article  CAS  PubMed  Google Scholar 

  68. Elser JJ, Stabler LB, Hassett RP (1995) Nutrient limitation of bacterial growth and rates of bacterivory in lakes and oceans: a comparative study. Aquat Microb Ecol 9:105–110. https://doi.org/10.3354/ame009105

    Article  Google Scholar 

  69. Eiler A, Langenheder S, Bertisson S, Tranvik LJ (2003) Heterotrophic bacterial growth efficiency and community structure at different natural organic carbon concentrations. Appl Environ Microbiol 69:3701–3709. https://doi.org/10.1128/AEM.69.7.3701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Dailloux M, Albert M, Laurain C, et al. (2003) Mycobacterium xenopi and drinking water biofilms. Appl Environ Microbiol 69:6946–6948. https://doi.org/10.1128/AEM.69.11.6946-6948.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Williams MM, Yakrus MA, Arduino MJ, et al. (2009) Structural analysis of biofilm formation by rapidly and slowly growing nontuberculous mycobacteria. Appl Environ Microbiol 75:2091–2098. https://doi.org/10.1128/AEM.00166-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Rosindell J, Hubbell SP, Etienne RS (2011) The unified neutral theory of biodiversity and biogeography at age ten. Trends Ecol Evol 26:340–348. https://doi.org/10.1016/j.tree.2011.03.024

    Article  PubMed  Google Scholar 

  73. Sloan WT, Lunn M, Woodcock S, et al. (2006) Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol 8:732–740. https://doi.org/10.1111/j.1462-2920.2005.00956.x

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the French National Research Agency through the PULSE (Peri-Urban Lakes, Society and Environment) research project (ANR-10-CEPL-010). Eau de Paris financed the mycobacterial analysis. The DSEA (Direction des Services de l’Environnement et de l’Assainissement) and the DGST (Direction Générale des Services Techniques), which belongs to the Departmental Council of the Val-de-Marne district, financed the equipment and monitoring of the storm sewer of Créteil Lake with a flowmeter. The DGST of Créteil City provided the authorizations and the street signalization equipment that were necessary to conduct the storm sewer study in Créteil Lake. We like to thank more specifically Mrs. Chamayou, Mrs. Vernin, Mrs. Berdoulay, and Mrs. Butel-Gomis. We are grateful to the stakeholders, owners, and municipalities for their authorizations to collect samples in each lake, and we especially thank the city of Créteil for their support. We also thank the leisure base of Créteil Lake for lending us their boats over the 2 years of sampling. Finally, we warmly thank all the colleagues who helped in sampling and quantifying the ecological parameters in the 49 lakes and Créteil Lake during these 2 years and the two anonymous reviewers whose comments improved the manuscript.

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  1. Adélaïde Roguet

    Present address: School of Freshwater Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, 53204, USA

Authors and Affiliations

  1. Leesu, UMR-MA 102, UPEC, École des Ponts, AgroParisTech, 94000, Créteil, France

    Adélaïde Roguet, Claire Therial, Adèle Bressy, Gilles Varrault, Lila Bouhdamane, Viet Tran, Bruno J. Lemaire, Brigitte Vincon-Leite, Mohamed Saad & Françoise S. Lucas

  2. Unité Molécules de Communication et Adaptation des Micro-organismes (MCAM UMR 7245), Sorbonne Université, Muséum National d’Histoire Naturelle, Case 39, 57 rue Cuvier, FR 75005, Paris, France

    Arnaud Catherine

  3. Eau de Paris, Direction Recherche et Développement Qualité de l’Eau (DRDQE), 33 avenue Jean Jaurès, FR 94200, Ivry-sur-Seine, France

    Laurent Moulin

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Roguet, A., Therial, C., Catherine, A. et al. Importance of Local and Regional Scales in Shaping Mycobacterial Abundance in Freshwater Lakes. Microb Ecol 75, 834–846 (2018). https://doi.org/10.1007/s00248-017-1088-6

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