A high-throughput sequencing ecotoxicology study of freshwater bacterial communities and their responses to tebuconazole

FEMS Microbiology Ecology

Volumn 90, Issue 3, 2014, Pages 563-574

  Pascault, Noémie ^a,b,c   Roux, Simon ^d,e   Artigas, Joan ^d,e,f   Pesce, Stéphane ^f   Leloup, Julie ^c   Tadonleke, Rémy D ^a,b   Debroas, Didier ^d,e   Bouchez, Agnès ^a,b   Humbert, Jean François ^c  

^a UMR CARRTEL   (France)

^b UNIVERSITÉ DE SAVOIE   (France)

^c UPMC University Paris 06   (France)

^d UNIVERSITÉ BLAISE PASCAL   (France)

^e UNIVERSITÉ CLERMONT AUVERGNE   (France)

^f UR MALY   (France)

Author keywords

NGS; Bacterial communities; Freshwater ecosystems; Pollutant; Tebuconazole

Indexed keywords

BACTERIA (MICROORGANISMS);

FUNGICIDE; RNA 16S; TEBUCONAZOLE; TRIAZOLE DERIVATIVE; WATER POLLUTANT;

ACTINOBACTERIA; DNA SEQUENCE; DRUG EFFECTS; ECOSYSTEM; ECOTOXICOLOGY; GAMMAPROTEOBACTERIA; GENETICS; HIGH THROUGHPUT SEQUENCING; LAKE; MICROBIAL CONSORTIUM; MICROBIOLOGY; MICROFLORA; NUCLEOTIDE SEQUENCE; RIVER; TOXICITY; WATER POLLUTANT;

ACTINOBACTERIA; BASE SEQUENCE; ECOSYSTEM; ECOTOXICOLOGY; FUNGICIDES, INDUSTRIAL; GAMMAPROTEOBACTERIA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LAKES; MICROBIAL CONSORTIA; MICROBIOTA; RIVERS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; TRIAZOLES; WATER POLLUTANTS;

EID: 84915770800     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12416     Document Type: Article

References (63)

1. Artigas J, Majerholc J, Foulquier A, Margoum C, Volat B, Neyra M & Pesce S (2012) Effects of the fungicide tebuconazole on microbial capacities for litter breakdown in streams. Aquat Toxicol 122-123: 197-205.
2. Artigas J, Pascault N, Bouchez A, Chastain J, Debroas D, Humbert JF, Leloup J, Tadonleke R, Ter Halle A & Pesce S (2014) Comparative sensitivity to the fungicide tebuconazole of biofilm and plankton microbial communities in freshwater ecosystems. Sci Total Environ 468-469: 326-336.
3. Atlas RM (1999) Minireview Legionella: from environmental habitats to disease pathology, detection and control. Environ Microbiol 1: 283-293.
4. Becher R, Hettwer U, Karlovsky P, Deising HB & Wirsel SGR (2010) Adaptation of Fusarium graminearum to tebuconazole yielded descendants diverging for levels of fitness, fungicide resistance, virulence, and mycotoxin production. Phytopathology 100: 444-453.
5. Bending GD, Rodriguez-Cruz MS & Lincoln SD (2007) Fungicide impacts on microbial communities in soils with contrasting management histories. Chemosphere 69: 82-88.
6. Besemer K, Peter H, Logue JB, Langenheder S, Lindström ES, Tranvik LJ & Battin TJ (2012) Unraveling assembly of stream biofilm communities. ISME J 6: 1459-1468.
7. Bricheux G, Morin L, Le Moal G, Coffe G, Balestrino D, Charbonnel N, Bohatier J & Forestier C (2013) Pyrosequencing assessment of prokaryotic and eukaryotic diversity in biofilm communities from a French river. Microbiologyopen 2: 402-414.
8. Chariton AA, Ho KT, Proestou D et al. (2014) A molecular-based approach for examining responses of eukaryotes in microcosms to contaminant-spiked estuarine sediments. Environ Toxicol Chem 33: 359-369.
9. Claesson MJ, Wang Q, O'Sullivan O, Greene-Diniz R, Cole JR, Ross RP & O'Toole PW (2010) Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res 38: e200.
10. Copping L & Hewitt H (1998) Chemistry and Mode of Action of Action of Crop Protection Agents. The Royal Society of Chemistry, Cambridge.
11. Cycon M, Piotrowska-Seget Z, Kaczynska A & Kozdroj J (2006) Microbiological characteristics of a sandy loam soil exposed to tebuconazole and k-cyhalothrin under laboratory conditions. Ecotoxicology 15: 639-646.
12. Debroas D, Humbert JF, Enault F, Bronner G, Faubladier M & Cornillot E (2009) Metagenomic approach studying the taxonomic and functional diversity of the bacterial community in a mesotrophic lake (Lac du Bourget-France). Environ Microbiol 11: 2412-2424.
13. Dijksterhuis J, van Doorn T, Samson R & Postma J (2011) Effects of seven fungicides on non-target aquatic fungi. Water Air Soil Pollut 222: 421-425.
14. dos Santos HF, Cury JC, do Carmo FL, dos Santos AL, Tiedje J, van Elsas JD, Rosado AS & Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS ONE 6: e16943.
15. Dray S, Dufour A & Chessel D (2007) The ade4 package-II: two-table and K-table methods. R News 7: 47-52.
16. Eddy S (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
17. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
18. Eiler A, Heinrich F & Bertilsson S (2012) Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6: 330-342.
19. Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459: 193-199.
20. Galand PE, Casamayor EO, Kirchman DL & Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. P Natl Acad Sci USA 106: 22427-22432.
21. Ge Y, Schimel JP & Holden PA (2012) Identification of soil bacteria susceptible to TiO2 and ZnO nanoparticles. Appl Environ Microbiol 78: 6749-6758.
22. Giongo A, Crabb DB, Davis-Richardson AG et al. (2010) PANGEA: pipeline for analysis of next generation amplicons. ISME J 4: 852-861.
23. Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A & Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Environ Microbiol 66: 5053-5065.
24. Hall EK, Besemer K, Kohl L, Preiler C, Riedel K, Schneider T, Wanek W & Battin TJ (2012) Effects of resource chemistry on the composition and function of stream hyporheic biofilms. Front Microbiol 3: 35.
25. Humbert JF, Dorigo U, Cecchi P, Le Berre B, Debroas D & Bouvy M (2009) Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ Microbiol 11: 2339-2350.
26. Jackson CJ, Lamb DC, Kelly DE & Kelly SL (2000) Bactericidal and inhibitory effects of azole antifungal compounds on Mycobacterium smegmatis. FEMS Microbiol Lett 192: 159-162.
27. Jackson CR, Churchill PF & Roden EE (2001) Successional changes in bacterial assemblage structure during epilithic biofilm development. Ecology 82: 555-566.
28. Kim Tiam S, Morin S, Pesce S, Feurtet-Mazel A, Moreira A, Gonzalez P & Mazzella N (2014) Environmental effects of realistic pesticide mixtures on natural biofilm communities with different exposure histories. Sci Total Environ 473-474: 496-506.
29. Knäbel A, Meyer K, Rapp J & Schulz R (2014) Fungicide field concentrations exceed FOCUS surface water predictions: urgent need of model improvement. Environ Sci Technol 48: 455-463.
30. Lozupone C & Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
31. Lyautey E, Jackson CR, Cayrou J, Rols JL & Garabétian F (2005) Bacterial community succession in natural river biofilm assemblages. Microb Ecol 50: 589-601.
32. Massana R, Murray A, Preston C & DeLong E (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63: 50-56.
33. Montuelle B, Dorigo U, Bérard A, Volat B, Bouchez A, Tlili A, Gouy V & Pesce S (2010) The periphyton as a multimetric bioindicator for assessing the impact of land use on rivers: an overview of the Ardières-Morcille experimental watershed. Hydrobiologia 657: 123-141.
34. Muñoz-Leoz B, Ruiz-Romera E, Antigüedad I & Garbisu C (2011) Tebuconazole application decreases soil microbial biomass and activity. Soil Biol Biochem 43: 2176-2183.
35. Newton RJ & McMahon KD (2011) Seasonal differences in bacterial community composition following nutrient additions in a eutrophic lake. Environ Microbiol 13: 887-899.
36. Obanda DN & Shupe TF (2009) Biotransformation of Tebuconazole by microorganisms: evidence of a common mechanism. Wood Fiber Sci 41: 157-167.
37. Parthuisot N, West NJ, Lebaron P & Baudart J (2010) High diversity and abundance of Legionella spp. in a pristine river and impact of seasonal and anthropogenic effects. Appl Environ Microbiol 76: 8201-8210.
38. Paver SF, Hayek KR, Gano KA et al. (2013) Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. Environ Microbiol 15: 2489-2504.
39. Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14: 257-263.
40. Pesce S, Fajon C, Bardot C, Bonnemoy F, Portelli C & Bohatier J (2008) Longitudinal changes in microbial planktonic communities of a French river in relation to pesticide and nutrient inputs. Aquat Toxicol 86: 352-360.
41. Pesce S, Martin-Laurent F, Rouard N, Robin A & Montuelle B (2010) Evidence for adaptation of riverine sediment microbial communities to diuron mineralization: incidence of runoff and soil erosion. J Soils Sediments 10: 698-707.
42. Pesce S, Bouchez A & Montuelle B (2011) Effects of organic herbicides on phototrophic microbial communities in freshwater ecosystems. Reviews of Environmental Contamination and Toxicology (Whitacre DM, ed.), pp. 87-124. Springer, New York, NY.
43. Price MN, Dehal PS & Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641-1650.
44. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
45. Rice P, Longden I & Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16: 276-277.
46. Richardson SD (2009) Water analysis: emerging contaminants and current issues. Anal Chem 81: 4645-4677.
47. Romani AM, Giorgi A, Acuna V & Sabater S (2004) The influence of substratum type and nutrient supply on biofilm organic matter utilization in streams. Limnol Oceanogr 49: 1713-1721.
48. Schauer M, Balague V, Pedros-Alio C & Massana R (2003) Seasonal changes in the taxonomic composition of bacterioplankton in a coastal oligotrophic system. Aquat Microb Ecol 31: 163-174.
49. Sehnem NT, Souza-Cruz P, Peralba MDCR & Zachia Ayub MA (2010) Biodegradation of tebuconazole by bacteria isolated from contaminated soils. J Environ Sci Health B 45: 67-72.
50. Sjöstedt J, Koch-Schmidt P, Pontarp M, Canbäck B, Tunlid A, Lundberg P, Hagström A & Riemann L (2012) Recruitment of members from the rare biosphere of marine bacterioplankton communities after an environmental disturbance. Appl Environ Microbiol 78: 1361-1369.
51. Strickland TC, Potter TL & Joo H (2004) Tebuconazole dissipation and metabolism in Tifton loamy sand during laboratory incubation. Pest Manag Sci 60: 703-709.
52. Tadonléké RD, Le Berre B, Perreau F & Humbert JF (2009) Responses of lake bacterioplankton activities and composition to the herbicide diuron. Aquat Toxicol 94: 103-113.
53. Taib N, Mangot JF, Domaizon I, Bronner G & Debroas D (2013) Phylogenetic affiliation of SSU rRNA genes generated by massively parallel sequencing: new insights into the freshwater protist diversity. PLoS ONE 8: e58950.
54. Tamames J, Abellán JJ, Pignatelli M, Camacho A & Moya A (2010) Environmental distribution of prokaryotic taxa. BMC Microbiol 10: 85.
55. Thevenon F, Graham ND, Herbez A, Wildi W & Poté J (2011) Spatio-temporal distribution of organic and inorganic pollutants from Lake Geneva (Switzerland) reveals strong interacting effects of sewage treatment plant and eutrophication on microbial abundance. Chemosphere 84: 609-617.
56. 3- dependence of the tolerance of autotrophic and heterotrophic biofilm communities to copper and diuron. Aquat Toxicol 98: 165-177.
57. Van Horn D, Sinsabaugh R, Takacs-Vesbach C, Mitchell K & Dahm C (2011) Response of heterotrophic stream biofilm communities to a gradient of resources. Aquat Microb Ecol 64: 149-161.
58. Verhagen P, De Gelder L, Hoefman S, De Vos P & Boon N (2011) Planktonic versus biofilm catabolic communities: importance of the biofilm for species selection and pesticide degradation RID B-4083-2011. Appl Environ Microbiol 77: 4728-4735.
59. Villeneuve A, Bouchez A & Montuelle B (2011) In situ interactions between the effects of season, current velocity and pollution on a river biofilm. Freshw Biol 56: 2245-2259.
60. Wallace DF & Dickinson DJ (2006) The bacterial transformation of organic biocides, a common mechanism? 37th Annual Meeting, Tromsø, Norway, pp. 1-7.
61. Wolinska A & Stepniewska Z (2012) Dehydrogenase activity in the soil environment. Biochemistry, Genetics and Molecular Biology 'Dehydrogenases' (Canuto RE, ed.), pp. 183-210. Intechopen, http: www.intechopen.com/books/dehydrogenases.
62. Zinger L, Gobet A & Pommier T (2012) Two decades of describing the unseen majority of aquatic microbial diversity. Mol Ecol 21: 1878-1896.
63. Zwart G, Crump BC, van Agterveld MPKV, Hagen F & Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28: 141-155.