Coaggregation occurs amongst bacteria within and between biofilms in domestic showerheads

Biofouling

Volumn 29, Issue 1, 2013, Pages 53-68

  Vornhagen, Jay ^a   Stevens, Michael ^a   McCormick, David W ^a   Dowd, Scot E ^b   Eisenberg, Joseph N S ^a   Boles, Blaise R ^a   Rickard, Alexander H ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b MR DNA Molecular Research LP   (United States)

Author keywords

autoaggregation; biofilm; coaggregation; phylogeny; pyrosequencing; showerhead

Indexed keywords

BACTERIA (MICROORGANISMS); BREVUNDIMONAS; LYSOBACTER; MICROCOCCUS;

BACTERIAL PROTEIN; FRESH WATER; RNA 16S; TITANIUM;

ARTICLE; BACTERIAL COUNT; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BACTERIUM ADHERENCE; BATH; BIOFILM; CHEMICAL PHENOMENA; CHEMISTRY; CLASSIFICATION; CONFOCAL MICROSCOPY; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; WATER SUPPLY;

BACTERIA; BACTERIAL ADHESION; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; BATHS; BIOFILMS; COLONY COUNT, MICROBIAL; FRESH WATER; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICROSCOPY, CONFOCAL; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TITANIUM; WATER SUPPLY;

EID: 84876436549     PISSN: 08927014     EISSN: 10292454     Source Type: Journal    
DOI: 10.1080/08927014.2012.744395     Document Type: Article

References (72)

1. Acosta-Martinez, V, Dowd, SE, Bell, CW, Lasconao, R, Booker, JD, Zobeck, TM, and Upchurch, DR. 2010. Microbial community composition as affected by dryland cropping systems and tillage in a semiarid sandy soil. Diversity, 2: 910–931.
2. Bailey, MT, Dowd, SE, Parry, NM, Galley, JD, Schauer, DB, and Lyte, M. 2010. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun, 78: 1509–1519.
3. Bauer, M, Mathieu, L, Deloge-Abarkan, M, Remen, T, Tossa, P, Hartemann, P, and Zmirou-Navier, D. 2008. Legionella bacteria in shower aerosols increase the risk of Pontiac fever among older people in retirement homes. J Epidemiol Community Health, 62: 913–920.
4. Bloetscher, F, Meeroff, DE, Pisani, JV, and Long, SC. 2010. Resolving problematic biofilms in buildings and compounds. Environ Eng Sci, 27: 767–776.
5. Bollin, GE, Plouffe, JF, Para, MF, and Hackman, B. 1985. Aerosols containing Legionella pneumophila generated by shower heads and hot-water faucets. Appl Environ Microbiol, 50: 1128–1131.
6. Buswell, CM, Herlihy, YM, Lawrence, LM, McGuiggan, JT, Marsh, PD, Keevil, CW, and Leach, SA. 1998. Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and -rRNA staining. Appl Environ Microbiol, 64: 733–741.
7. Callaway, TR, Dowd, SE, Edrington, TS, Anderson, RC, Krueger, N, Bauer, N, Kononoff, PJ, and Nisbet, DJ. 2010. Evaluation of bacterial diversity in the rumen and feces of cattle fed diets containing levels of dried distiller's grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). J Anim Sci, 88: 3977–3983.
8. Camper, A, Burr, M, Ellis, B, Butterfield, P, and Abernathy, C. 1998. Development and structure of drinking water biofilms and techniques for their study. J Appl Microbiol, 85 (Suppl 1): 1S–12S.
9. Capone, KA, Dowd, SE, Stamatas, GN, and Nikolovski, J. 2011. Diversity of the human skin microbiome early in life. J Invest Dermatol, 131: 2026–2032.
10. Caporaso, JG, Kuczynski, J, Stombaugh, J, Bittinger, K, Bushman, FD, Costello, EK, Fierer, N, Pena, AG, Goodrich, JK, Gordon, JI. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods, 7: 335–336.
11. Chauvet, LP, Probert, SD, and Nevrala, DJ. 1994. Thermal-energy stores for supplying domestic hot-water and space-heating. Appl Energy, 48: 163–190.
12. Chen, X, Tian, F, Liu, X, Zhao, J, Zhang, HP, Zhang, H, and Chen, W. 2010. In vitro screening of lactobacilli with antagonistic activity against Helicobacter pylori from traditionally fermented foods. J Dairy Sci, 93: 5627–5634.
13. Cheng, SM, and Foght, JM. 2007. Cultivation-independent and -dependent characterization of bacteria resident beneath John Evans Glacier. FEMS Microbiol Ecol, 59: 318–330.
14. Christensen, P, and Cook, FD. 1978. Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. Int J Syst Bacteriol, 28: 367–393.
15. Cisar, JO, Kolenbrander, PE, and McIntire, FC. 1979. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun, 24: 742–752.
16. Cooksey, RC, Jhung, MA, Yakrus, MA, Butler, WR, Adekambi, T, Morlock, GP, Williams, M, Shams, AM, Jensen, BJ, Morey, RE. 2008. Multiphasic approach reveals genetic diversity of environmental and patient isolates of Mycobacterium mucogenicum and Mycobacterium phocaicum associated with an outbreak of bacteremias at a Texas hospital. Appl Environ Microbiol, 74: 2480–2487.
17. Costerton, JW, Lewandowski, Z, Caldwell, DE, Korber, DR, and Lappin-Scott, HM. 1995. Microbial biofilms. Annu Rev Microbiol, 49: 711–745.
18. Dowd, SE, Wolcott, RD, Sun, Y, McKeehan, T, Smith, E, and Rhoads, D. 2008. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One, 3: e3326
19. Edgar, RC, Haas, BJ, Clemente, JC, Quince, C, and Knight, R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27: 2194–2200.
20. Elliott, DR, Wilson, M, Buckley, CM, and Spratt, DA. 2006. Aggregative behavior of bacteria isolated from canine dental plaque. Appl Environ Microbiol, 72: 5211–5217.
21. Exner, M, Kramer, A, Lajoie, L, Gebel, J, Engelhart, S, and Hartemann, P. 2005. Prevention and control of health care-associated waterborne infections in health care facilities. Am J Infect Control, 33: S26–S2640.
22. Falkinham, JO, 3rd, Iseman, MD, de Haas, P, and van Soolingen, D. 2008. Mycobacterium avium in a shower linked to pulmonary disease. J Water Health, 6: 209–213.
23. Feazel, LM, Baumgartner, LK, Peterson, KL, Frank, DN, Harris, JK, and Pace, NR. 2009. Opportunistic pathogens enriched in showerhead biofilms. P Natl Acad Sci USA, 106: 16393–16399.
24. Ferroni, A, Werkhauser-Bertrand, A, Le Bourgeois, M, Beauvais, R, Vrielynck, S, Durand, C, Lenoir, G, Berche, P, and Sermet-Gaudelus, I. 2008. Bacterial contamination in the environment of hospitalised children with cystic fibrosis. J Cyst Fibros, 7: 477–482.
25. Gibbons, RJ, and Nygaard, M. 1970. Interbacterial aggregation of plaque bacteria. Arch Oral Biol, 15: 1397–1400.
26. Guss, AM, Roeselers, G, Newton, IL, Young, CR, Klepac-Ceraj, V, Lory, S, and Cavanaugh, CM. 2010. Phylogenetic and metabolic diversity of bacteria associated with cystic fibrosis. ISME J, 5: 20–29.
27. Handl, S, Dowd, SE, Garcia-Mazcorro, JF, Steiner, JM, and Suchodolski, JS. 2011. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol, 76: 301–310.
28. Hayward, AC, Fegan, N, Fegan, M, and Stirling, GR. 2010. Stenotrophomonas and Lysobacter: ubiquitous plant-associated gamma-proteobacteria of developing significance in applied microbiology. J Appl Microbiol, 108: 756–770.
29. Hojo, K, Nagaoka, S, Ohshima, T, and Maeda, N. 2009. Bacterial interactions in dental biofilm development. J Dent Res, 88: 982–990.
30. Ishak, HD, Plowes, R, Sen, R, Kellner, K, Meyer, E, Estrada, DA, Dowd, SE, and Mueller, UG. 2011. Bacterial diversity in Solenopsis invicta and Solenopsis geminata ant colonies characterized by 16S amplicon 454 pyrosequencing. Microb Ecol, 61: 821–831.
31. Jakubovics, NS, Gill, SR, Iobst, SE, Vickerman, MM, and Kolenbrander, PE. 2008a. Regulation of gene expression in a mixed-genus community: stabilized arginine biosynthesis in Streptococcus gordonii by coaggregation with Actinomyces naeslundii. J Bacteriol, 190: 3646–3657.
32. Jakubovics, NS, Gill, SR, Vickerman, MM, and Kolenbrander, PE. 2008b. Role of hydrogen peroxide in competition and cooperation between Streptococcus gordonii and Actinomyces naeslundii. FEMS Microbiol Ecol, 66: 637–644.
33. Jukes, TH, and Cantor, CR. 1969. “ Evolution of protein molecules ”. In Mammalian, Edited by: Munro, HN. 21–132. New York, NY: Academic Press Inc; p.
34. Keinanen, MM, Korhonen, LK, Lehtola, MJ, Miettinen, IT, Martikainen, PJ, Vartiainen, T, and Suutari, MH. 2002. The microbial community structure of drinking water biofilms can be affected by phosphorus availability. Appl Environ Microbiol, 68: 434–439.
35. Khemaleelakul, S, Baumgartner, JC, and Pruksakom, S. 2006. Autoaggregation and coaggregation of bacteria associated with acute endodontic infections. J Endod, 32: 312–318.
36. Kolenbrander, PE. 2000. Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol, 54: 413–437.
37. Kolenbrander, PE, Palmer, RJ, Jr., Periasamy, S, and Jakubovics, NS. 2010. Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol, 8: 471–480.
38. Kolenbrander, PE, Palmer, RJ, Jr, Rickard, AH, Jakubovics, NS, Chalmers, NI, and Diaz, PI. 2006. Bacterial interactions and successions during plaque development. Periodontol. 2000, 42: 47–79.
39. Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23: 2947–2948.
40. Ledder, RG, Timperley, AS, Friswell, MK, Macfarlane, S, and McBain, AJ. 2008. Coaggregation between and among human intestinal and oral bacteria. FEMS Microbiol Ecol, 66: 630–636.
41. Luthje, P, and Brauner, A. 2010. Ag43 promotes persistence of uropathogenic Escherichia coli isolates in the urinary tract. J Clin Microbiol, 48: 2316–2317.
42. Lyautey, E, Jackson, CR, Cayrou, J, Rols, JL, and Garabetian, F. 2005. Bacterial community succession in natural river biofilm assemblages. Microb Ecol, 50: 589–601.
43. Marras, TK, Wallace, RJ, Jr, Koth, LL, Stulbarg, MS, Cowl, CT, and Daley, CL. 2005. Hypersensitivity pneumonitis reaction to Mycobacterium avium in household water. Chest, 127: 664–671.
44. Massa, S, Caruso, M, Trovatelli, F, and Tosques, M. 1998. Comparison of plate count agar and R2A medium for enumeration of heterotrophic bacteria in natural mineral water World. J Microbiol Biotechnol, 14: 727–730.
45. McCormick, DW, Stevens, MRE, Boles, BR, and Rickard, AH. 2011. Does it take two to tango? The importance of coaggregation in multi-species biofilms. Culture, 32: 1–5.
46. McMillan, A, Dell, M, Zellar, MP, Cribby, S, Martz, S, Hong, E, Fu, J, Abbas, A, Dang, T, Miller, W, and Reid, G. 2011. Disruption of urogenital biofilms by lactobacilli. Colloids Surf B Biointerfaces, 86: 58–64.
47. Merritt, J, Niu, G, Okinaga, T, and Qi, F. 2009. Autoaggregation response of Fusobacterium nucleatum. Appl Environ Microbiol, 75: 7725–7733.
48. Min, KR, and Rickard, AH. 2009. Coaggregation by the freshwater bacterium Sphingomonas natatoria alters dual-species biofilm formation. Appl Environ Microbiol, 75: 3987–3997.
49. Min, KR, Zimmer, MN, and Rickard, AH. 2010. Physicochemical parameters influencing coaggregation between the freshwater bacteria Sphingomonas natatoria 2.1 and Micrococcus luteus 2.13. Biofouling, 26: 931–940.
50. Na, H, Kim, OS, Yoon, SH, Kim, Y, and Chun, J. 2011. Comparative approach to capture bacterial diversity of coastal waters. J Microbiol, 49: 729–740.
51. Nishiuchi, Y, Tamura, A, Kitada, S, Taguri, T, Matsumoto, S, Tateishi, Y, Yoshimura, M, Ozeki, Y, Matsumura, N, Ogura, H, and Maekura, R. 2009. Mycobacterium aviumz complex organisms predominantly colonize in the bathtub inlets of patients' bathrooms. Jpn J Infect Dis, 62: 182–186.
52. Percival, SL, Knapp, JS, Edyvean, R, and Wales, DS. 1988. Biofilm development on stainless steel in mains water. Water Res, 32: 243–253.
53. Pitta, DW, Pinchak, E, Dowd, SE, Osterstock, J, Gontcharova, V, Youn, E, Dorton, K, Yoon, I, Min, BR, Fulford, JD. 2010. Rumen bacterial diversity dynamics associated with changing from bermudagrass hay to grazed winter wheat diets. Microb Ecol, 59: 511–522.
54. Reasoner, DJ, and Geldreich, EE. 1985. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol, 49: 1–7.
55. Reid, G, McGroarty, JA, Angotti, R, and Cook, RL. 1988. Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Can J Microbiol, 34: 344–351.
56. Rickard, AH, Gilbert, P, High, NJ, Kolenbrander, PE, and Handley, PS. 2003a. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol, 11: 94–100.
57. Rickard, AH, Leach, SA, Buswell, CM, High, NJ, and Handley, PS. 2000. Coaggregation between aquatic bacteria is mediated by specific-growth-phase-dependent lectin-saccharide interactions. Appl Environ Microbiol, 66: 431–434.
58. Rickard, AH, Leach, SA, Hall, LS, Buswell, CM, High, NJ, and Handley, PS. 2002. Phylogenetic relationships and coaggregation ability of freshwater biofilm bacteria. Appl Environ Microbiol, 68: 3644–3650.
59. Rickard, AH, McBain, AJ, Ledder, RG, Handley, PS, and Gilbert, P. 2003b. Coaggregation between freshwater bacteria within biofilm and planktonic communities. FEMS Microbiol Lett, 220: 133–140.
60. Rickard, AH, McBain, AJ, Stead, AT, and Gilbert, P. 2004. Shear rate moderates community diversity in freshwater biofilms. Appl Environ Microbiol, 70: 7426–7435.
61. Rochex, A, Godon, JJ, Bernet, N, and Escudie, R. 2008. Role of shear stress on composition, diversity and dynamics of biofilm bacterial communities. Water Res, 42: 4915–4922.
62. Rosenberg, M. 1981. Bacterial adherence to polystyrene: a replica method of screening for bacterial hydrophobicity. Appl Environ Microbiol, 42: 375–377.
63. Rosenberg, M, and Rosenberg, E. 1981. Role of adherence in growth of Acinetobacter calcoaceticus RAG-1 on hexadecane. J Bacteriol, 148: 51–57.
64. Schloss, PD, and Handelsman, J. 2005. Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol, 6: 229.
65. Schoen, ME, and Ashbolt, NJ. 2011. An in-premise model for Legionella exposure during showering events. Water Res, 45: 5826–5836.
66. Schwartz, T, Hoffmann, S, and Obst, U. 1998. Formation and bacterialcomposition of young, natural biofilms obtained from public bank-filtered drinking water systems. Water Res, 32: 2787–2797.
67. Simoes, LC, Simoes, M, and Vieira, MJ. 2008. Intergeneric coaggregation among drinking water bacteria: evidence of a role for Acinetobacter calcoaceticus as a bridging bacterium. Appl Environ Microbiol, 74: 1259–1263.
68. Spiegelman, D, Whissell, G, and Greer, CW. 2005. A survey of the methods for the characterization of microbial consortia and communities. Can J Microbiol, 51: 355–386.
69. Van de Peer, Y, and De Wachter, R. 1993. TREECON: a software package for the construction and drawing of evolutionary trees. Comput Appl Biosci, 9: 177–182.
70. Van Houdt, R, and Michiels, CW. 2005. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res Microbiol, 156: 626–633.
71. Walter, J, Schwab, C, Loach, DM, Ganzle, MG, and Tannock, GW. 2008. Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. Microbiology, 154: 72–80.
72. Whitmore, SE, and Lamont, RJ. 2011. The pathogenic persona of community-associated oral streptococci. Mol Microbiol, 81: 305–314.