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Materials and Structures

, 50:25 | Cite as

Analysis of bacterial communities in and on concrete

Original Article

Abstract

Bacteria are known to catalyze degradation of concrete, and have more recently been used to repair micro-cracks in or form protective biofilms on cement mortar. However, the microbial communities in and on concrete under ordinary weathering conditions have not been characterized, in part because of difficulty in extracting DNA from inside concrete specimens. Here, we report a method for extraction of nucleic acids directly from hardened concrete. Using this method and classical cultivation methods, we demonstrate that most bacteria in or on concrete belong to two taxonomic groups, that the bacterial diversity is similar on the concrete surface and in the interior, and that many bacteria in and on concrete are related to microbes found in other dry, saline, or alkaline environments. This method lays the foundation for the creation of bioindicators for concrete and may open new avenues for the fields of non-destructive evaluation and assessment of concrete structures.

Keywords

Bacteria Concrete Bioindicator Non-destructive evaluation 

Notes

Acknowledgments

This work was supported by grant # 12A01559 from the University of Delaware Research Foundation to JAM and TS. Additional support was provided by the Mid-Atlantic Transportation Sustainability University Transportation Center (MATS UTC). MATS UTC is funded by grant # DTRT13-G-UTC33 from the US Department of Transportation and matching funds organized by the Delaware Center for Transportation. We thank Keira Zhang for assistance with concrete processing. Additionally, the authors gratefully acknowledge Dr. Deborah Powell at the University of Delaware BioImaging Center for assistance with the SEM/EDS analysis, Dr. Brewster Kingham at the University of Delaware Sequencing and Genotyping Center for sequencing of the 16S rRNA genes of the isolates and the Research and Testing Laboratories in Lubbock, TX, for amplicon sequencing of the 16S rRNA genes from DNA extracted directly from concrete. We thank David Dodd at the Delaware Department of Transportation for concrete materials and mix designs, Dr. Jennifer Biddle and Dr. Farshad Rajabipoor for helpful discussions, and Gary Wenczel, Michael Davidson, and Dr. Jessica Keffer for technical assistance.

Supplementary material

11527_2016_929_MOESM1_ESM.docx (177 kb)
Supplementary material 1 (DOCX 176 kb)

References

  1. 1.
    Arndt RW, Schumacher T, Algernon D, Kee S-H (2011) Strategies for maintenance of highway bridges in the US-with the support of nondestructive testing and structural health monitoring. Bautechnik 88:793–804CrossRefGoogle Scholar
  2. 2.
    Amini K, Kraatz H-B (2014) Recent advances and developments in monitoring biological agents in water samples. Rev Environ Sci Bio/Technol 14:23–48. doi: 10.1007/s11157-014-9351-5 CrossRefGoogle Scholar
  3. 3.
    Marine SC, Pagadala S, Wang F, Pahl DM, Melendez MV, Kline WL, Oni RA, Walsh CS, Everts KL, Buchanan RL, Micallef SA (2015) The growing season, but not the farming system, is a food safety risk determinant for leafy greens in the mid-Atlantic region of the United States. Appl Environ Microbiol 81:2395–2407. doi: 10.1128/AEM.00051-15 CrossRefGoogle Scholar
  4. 4.
    O’Connell M, McNally C, Richardson MG (2010) Biochemical attack on concrete in wastewater applications: a state of the art review. Cem Concr Compos 32:479–485. doi: 10.1016/j.cemconcomp.2010.05.001 CrossRefGoogle Scholar
  5. 5.
    Wei S, Sanchez M, Trejo D, Gillis C (2010) Microbial mediated deterioration of reinforced concrete structures. Int Biodeterior Biodegrad 64:748–754. doi: 10.1016/j.ibiod.2010.09.001 CrossRefGoogle Scholar
  6. 6.
    Wei S, Jiang Z, Liu H, Zhou D, Sanchez-Silva M (2013) Microbiologically induced deterioration of concrete—a review. Braz J Microbiol 44:1001–1007. doi: 10.1590/S1517-83822014005000006 CrossRefGoogle Scholar
  7. 7.
    Jonkers HM, Thijssen A, Muyzer G, Copuroglu O, Schlangen E (2010) Application of bacteria as self-healing agent for the development of sustainable concrete. Ecol Eng 36:230–235CrossRefGoogle Scholar
  8. 8.
    Van Tittelboom K, De Belie N, De Muynck W, Verstraete W (2010) Use of bacteria to repair cracks in concrete. Cem Concr Res 40:157–166CrossRefGoogle Scholar
  9. 9.
    De Muynck W, De Belie N, Verstraete W (2010) Microbial carbonate precipitation in construction materials: a review. Ecol Eng 36:118–136. doi: 10.1016/j.ecoleng.2009.02.006 CrossRefGoogle Scholar
  10. 10.
    Okabe S, Odagiri M, Ito T, Satoh H (2007) Succession of sulfur-oxidizing bacteria in the microbial community on corroding concrete in sewer systems. Appl Environ Microbiol 73:971–980. doi: 10.1128/AEM.02054-06 CrossRefGoogle Scholar
  11. 11.
    Taylor CB, Hutchinson GH (1947) Corrosion of concrete caused by sulphur-oxidising bacteria. J Soc Chem Ind 66:54–57. doi: 10.1002/jctb.5000660205 CrossRefGoogle Scholar
  12. 12.
    Trejo D, de Figueiredo P, Sanchez M, Gonzalez C, Shiping W, Li L (2008) Analysis and assessment of microbial biofilm-mediated concrete deterioration. Texas Transportation Institute, College StationGoogle Scholar
  13. 13.
    Gu J-D, Ford TE, Mitchell R (2011) Microbiological corrosion of concrete. In: Revie RW (ed) Uhlig’s corrosion handbook, 3rd edn. Wiley, New York, pp 451–460CrossRefGoogle Scholar
  14. 14.
    Gomez-Alvarez V, Revetta RP, Santo Domingo JW (2012) Metagenome analyses of corroded concrete wastewater pipe biofilms reveal a complex microbial system. BMC Microbiol 12:122. doi: 10.1186/1471-2180-12-122 CrossRefGoogle Scholar
  15. 15.
    Ling AL, Robertson CE, Harris JK, Frank DN, Kotter CV, Stevens MJ, Pace NR, Hernandez MT (2014) Carbon dioxide and hydrogen sulfide associations with regional bacterial diversity patterns in microbially induced concrete corrosion. Environ Sci Technol 48:7357–7364. doi: 10.1021/es500763e CrossRefGoogle Scholar
  16. 16.
    Gomez-Alvarez V (2014) Biofilm-growing bacteria involved in the corrosion of concrete wastewater pipes: protocols for comparative metagenomic analyses. Methods Mol Biol 1147:323–340. doi: 10.1007/978-1-4939-0467-9_23 CrossRefGoogle Scholar
  17. 17.
    Ling AL, Robertson CE, Harris JK, Frank DN, Kotter CV, Stevens MJ, Pace NR, Hernandez MT (2015) High-resolution microbial community succession of microbially induced concrete corrosion in working sanitary manholes. PLoS One 10:e0116400. doi: 10.1371/journal.pone.0116400 CrossRefGoogle Scholar
  18. 18.
    De Muynck W, Cox K, De Belie N, Verstraete W (2008) Bacterial carbonate precipitation as an alternative surface treatment for concrete. Constr Build Mater 22:875–885. doi: 10.1016/j.conbuildmat.2006.12.011 CrossRefGoogle Scholar
  19. 19.
    Jonkers HM, Schlangen E (2007) Crack repair by concrete-immobilized bacteria. In: Proceedings of the first international conference on self healing materialsGoogle Scholar
  20. 20.
    Lv J, Mao J, Ba H (2015) Influence of marine microorganisms on the permeability and microstructure of mortar. Constr Build Mater 77:33–40. doi: 10.1016/j.conbuildmat.2014.11.072 CrossRefGoogle Scholar
  21. 21.
    Berndt ML (2011) Evaluation of coatings, mortars and mix design for protection of concrete against sulphur oxidising bacteria. Constr Build Mater 25:3893–3902. doi: 10.1016/j.conbuildmat.2011.04.014 CrossRefGoogle Scholar
  22. 22.
    Soleimani S, Ormeci B, Isgor OB (2013) Growth and characterization of Escherichia coli DH5α biofilm on concrete surfaces as a protective layer against microbiologically influenced concrete deterioration (MICD). Appl Microbiol Biotechnol 97:1093–1102. doi: 10.1007/s00253-012-4379-3 CrossRefGoogle Scholar
  23. 23.
    Wolin EA, Wolin MJ, Wolfe RS (1963) Formation of methane by bacterial extracts. J Biol Chem 238:2882–2886Google Scholar
  24. 24.
    Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338. doi: 10.1111/j.1550-7408.1999.tb04612.x CrossRefGoogle Scholar
  25. 25.
    Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  26. 26.
    Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376Google Scholar
  27. 27.
    Cattaneo C, Smillie DM, Gelsthorpe K, Piccinini A, Gelsthorpe AR, Sokol RJ (1995) A simple method for extracting DNA from old skeletal material. Forensic Sci Int 74:167–174. doi: 10.1016/0379-0738(95)01758-B CrossRefGoogle Scholar
  28. 28.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi: 10.1038/ismej.2012.8 CrossRefGoogle Scholar
  29. 29.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Peña A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi: 10.1038/nmeth.f.303 CrossRefGoogle Scholar
  30. 30.
    Aronesty E (2013) Comparison of sequencing utility programs. Open Bioinform J 7:1–8MathSciNetCrossRefGoogle Scholar
  31. 31.
    Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R (2012) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Microbiol Chapter 1:Unit 1E.5. doi:  10.1002/9780471729259.mc01e05s27
  32. 32.
    Yamanaka T, Aso I, Togashi S, Tanigawa M, Shoji K, Watanabe T, Watanabe N, Maki K, Suzuki H (2002) Corrosion by bacteria of concrete in sewerage systems and inhibitory effects of formates on their growth. Water Res 36:2636–2642. doi: 10.1016/S0043-1354(01)00473-0 CrossRefGoogle Scholar
  33. 33.
    Kim SB, Nedashkovskaya OI, Mikhailov VV, Han SK, Kim K-O, Rhee M-S, Bae KS (2004) Kocuria marina sp. nov., a novel actinobacterium isolated from marine sediment. Int J Syst Evol Microbiol 54:1617–1620. doi: 10.1099/ijs.0.02742-0 CrossRefGoogle Scholar
  34. 34.
    Sarafin Y, Donio MBS, Velmurugan S, Michaelbabu M, Citarasu T (2014) Kocuria marina BS-15 a biosurfactant producing halophilic bacteria isolated from solar salt works in India. Saudi J Biol Sci 21:511–519. doi: 10.1016/j.sjbs.2014.01.001 CrossRefGoogle Scholar
  35. 35.
    Duckworth A, Grant S, Grant W, Jones BE, Meijer D (1998) Dietzia natronolimnaios sp. nov., a new member of the genus Dietzia isolated from an East African soda lake. Extremophiles 2:359–366CrossRefGoogle Scholar
  36. 36.
    Yoon J-H, Lee C-H, Oh T-K (2006) Nocardioides lentus sp. nov., isolated from an alkaline soil. Int J Syst Evol Microbiol 56:271–275. doi: 10.1099/ijs.0.63993-0 CrossRefGoogle Scholar
  37. 37.
    Loreille OM, Diegoli TM, Irwin JA, Coble MD, Parsons TJ (2007) High efficiency DNA extraction from bone by total demineralization. Forensic Sci Int Genet 1:191–195. doi: 10.1016/j.fsigen.2007.02.006 CrossRefGoogle Scholar
  38. 38.
    Reysenbach AL, Wickham GS, Pace NR (1994) Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. Appl Environ Microbiol 60:2113–2119Google Scholar
  39. 39.
    Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290. doi: 10.1038/ismej.2007.53 Google Scholar
  40. 40.
    Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631. doi: 10.1111/j.1462-2920.2007.01301.x CrossRefGoogle Scholar
  41. 41.
    Rolleke S, Muyzer G, Wawer C, Wanner G, Lubitz W (1996) Identification of bacteria in a biodegraded wall painting by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 62:2059–2065Google Scholar
  42. 42.
    McNamara CJ, Perry TD, Bearce KA, Hernandez-Duque G, Mitchell R (2006) Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. Microb Ecol 51:51–64. doi: 10.1007/s00248-005-0200-5 CrossRefGoogle Scholar
  43. 43.
    Ramírez M, Hernández-Mariné M, Novelo E, Roldán M (2010) Cyanobacteria-containing biofilms from a Mayan monument in Palenque, Mexico. Biofouling 26:399–409CrossRefGoogle Scholar
  44. 44.
    Suihko M-L, Alakomi H-L, Gorbushina A, Fortune I, Marquardt J, Saarela M (2007) Characterization of aerobic bacterial and fungal microbiota on surfaces of historic Scottish monuments. Syst Appl Microbiol 30:494–508. doi: 10.1016/j.syapm.2007.05.001 CrossRefGoogle Scholar
  45. 45.
    Gaylarde CC, Gaylarde PM, Beech IB (2008) Deterioration of limestone structures associated with copper staining. Int Biodeterior Biodegrad 62:179–185. doi: 10.1016/j.ibiod.2008.01.007 CrossRefGoogle Scholar
  46. 46.
    Normand P, Daffonchio D, Gtari M (2014) The family Geodermatophilaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, pp 361–379Google Scholar
  47. 47.
    Urzi C, Brusetti L, Salamone P, Sorlini C, Stackebrandt E, Daffonchio D (2001) Biodiversity of Geodermatophilaceae isolated from altered stones and monuments in the Mediterranean basin. Environ Microbiol 3:471–479. doi: 10.1046/j.1462-2920.2001.00217.x CrossRefGoogle Scholar
  48. 48.
    Weon H-Y, Kim B-Y, Hong S-B, Joa J-H, Nam S-S, Lee KH, Kwon S-W (2007) Skermanella aerolata sp. nov., isolated from air, and emended description of the genus Skermanella. Int J Syst Evol Microbiol 57:1539–1542. doi: 10.1099/ijs.0.64676-0 CrossRefGoogle Scholar
  49. 49.
    An H, Zhang L, Tang Y, Luo X, Sun T, Li Y, Wang Y, Dai J, Fang C (2009) Skermanella xinjiangensis sp. nov., isolated from the desert of Xinjiang, China. Int J Syst Evol Microbiol 59:1531–1534. doi: 10.1099/ijs.0.003350-0 CrossRefGoogle Scholar
  50. 50.
    Luo G, Shi Z, Wang H, Wang G (2012) Skermanella stibiiresistens sp. nov., a highly antimony-resistant bacterium isolated from coal-mining soil, and emended description of the genus Skermanella. Int J Syst Evol Microbiol 62:1271–1276. doi: 10.1099/ijs.0.033746-0 CrossRefGoogle Scholar
  51. 51.
    Cayford BI, Dennis PG, Keller J, Tyson GW, Bond PL (2012) High-throughput amplicon sequencing reveals distinct communities within a corroding concrete sewer system. Appl Environ Microbiol 78:7160–7162CrossRefGoogle Scholar
  52. 52.
    Vupputuri S, Fathepure BZ, Wilber GG, Sudoi E, Nasrazadani S, Ley MT, Ramsey JD (2015) Isolation of a sulfur-oxidizing Streptomyces sp. from deteriorating bridge structures and its role in concrete deterioration. Int Biodeterior Biodegrad 97:128–134. doi: 10.1016/j.ibiod.2014.11.002 CrossRefGoogle Scholar
  53. 53.
    Lu J, Santo Domingo JW, Lamendella R, Edge T, Hill S (2008) Phylogenetic diversity and molecular detection of bacteria in gull feces. Appl Environ Microbiol 74:3969–3976. doi: 10.1128/AEM.00019-08 CrossRefGoogle Scholar
  54. 54.
    Green HC, Dick LK, Gilpin B, Samadpour M, Field KG (2012) Genetic markers for rapid PCR-based identification of gull, Canada goose, duck, and chicken fecal contamination in water. Appl Environ Microbiol 78:503–510. doi: 10.1128/AEM.05734-11 CrossRefGoogle Scholar
  55. 55.
    Demkina EV, Soina VS, Registan GIE, Zvyagintsev DG (2000) Reproductive resting forms ofArthrobacter globiformis. Microbiology 69:309–313. doi: 10.1007/BF02756739 CrossRefGoogle Scholar
  56. 56.
    Shimkets LJ (2013) Prokaryotic life cycles. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) Prokaryotes prokaryotic communities ecophysiol. Springer, Berlin, pp 317–336Google Scholar
  57. 57.
    Young M, Artsatbanov V, Beller HR, Chandra G, Chater KF, Dover LG, Goh E-B, Kahan T, Kaprelyants AS, Kyrpides N, Lapidus A, Lowry SR, Lykidis A, Mahillon J, Markowitz V, Mavromatis K, Mukamolova GV, Oren A, Rokem JS, Smith MCM, Young DI, Greenblatt CL (2010) Genome sequence of the Fleming strain of Micrococcus luteus, a simple free-living actinobacterium. J Bacteriol 192:841–860. doi: 10.1128/JB.01254-09 CrossRefGoogle Scholar
  58. 58.
    Fong NJC, Burgess ML, Barrow KD, Glenn DR (2001) Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress. Appl Microbiol Biotechnol 56:750–756. doi: 10.1007/s002530100739 CrossRefGoogle Scholar
  59. 59.
    Giannantonio DJ, Kurth JC, Kurtis KE, Sobecky PA (2009) Molecular characterizations of microbial communities fouling painted and unpainted concrete structures. Int Biodeterior Biodegrad 63:30–40. doi: 10.1016/j.ibiod.2008.06.004 CrossRefGoogle Scholar
  60. 60.
    Epstein S (2013) The phenomenon of microbial uncultivability. Curr Opin Microbiol 16:636–642. doi: 10.1016/j.mib.2013.08.003 CrossRefGoogle Scholar
  61. 61.
    Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270MathSciNetGoogle Scholar
  62. 62.
    Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci 345:101–118. doi: 10.1098/rstb.1994.0091 CrossRefGoogle Scholar

Copyright information

© RILEM 2016

Authors and Affiliations

  1. 1.Department of Civil and Environmental EngineeringUniversity of DelawareNewarkUSA
  2. 2.Department of Civil and Environmental EngineeringPortland State UniversityPortlandUSA

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