Abstract
With the rapid advances in sequencing technology, the cost of sequencing has dramatically dropped and the scale of sequencing projects has increased accordingly. This has provided the opportunity for the routine use of sequencing techniques in the monitoring of environmental microbes. While metagenomic applications have been routinely applied to better understand the ecology and diversity of microbes, their use in environmental monitoring and bioremediation is increasingly common. In this review we seek to provide an overview of some of the metagenomic techniques used in environmental systems biology, addressing their application and limitation. We will also provide several recent examples of the application of metagenomics to bioremediation. We discuss examples where microbial communities have been used to predict the presence and extent of contamination, examples of how metagenomics can be used to characterize the process of natural attenuation by unculturable microbes, as well as examples detailing the use of metagenomics to understand the impact of biostimulation on microbial communities.
Similar content being viewed by others
References
Chakraborty R, Wu CH, Hazen TC (2012) Systems biology approach to bioremediation. Curr Opin Biotechnol 23:483–490. doi:10.1016/j.copbio.2012.01.015
Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:35–44. doi:10.1038/nrmicro731
Payne RB, May HD, Sowers KR (2011) Enhanced reductive dechlorination of polychlorinated biphenyl impacted sediment by bioaugmentation with a dehalorespiring bacterium. Environ Sci Technol 45:8772–8779
Salanitro JP, Johnson PC, Spinnler GE, Maner PM, Wisniewski HL, Bruce C (2000) Field-scale demonstration of enhanced MTBE bioremediation through aquifer bioaugmentation and oxygenation. Environ Sci Technol 34:4152–4162
Klipp E, Liebermeister W, Wierling C, Kowald A, Herwig R (2016) Systems biology: a textbook. Wiley, New York
Hazen TC, Sayler GS (2016) Environmental systems microbiology of contaminated environments. In: Yates M, Nakatsu C, Miller RSP (eds) Manual of environmental microbiology, vol 4th edn. ASM Press, Washington, DC, pp 5.1.6-1–5.1.6-10
Alivisatos AP, Blaser MJ, Brodie EL, Chun M, Dangl JL, Donohue TJ, Dorrestein PC, Gilbert JA, Green JL, Jansson JK, Knight R, Maxon ME, McFall-Ngai MJ, Miller JF, Pollard KS, Ruby EG, Taha SA (2015) A unified initiative to harness Earth’s microbiomes. Science 350:507–508. doi:10.1126/science.aac8480
Shade A, Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14:4–12. doi:10.1111/j.1462-2920.2011.02585.x
Smith MB, Rocha AM, Smillie CS, Olesen SW, Paradis C, Wu L, Campbell JH, Fortney JL, Mehlhorn TL, Lowe KA (2015) Natural bacterial communities serve as quantitative geochemical biosensors. Mbio 6:e00326–e00335
Hazen TC, Rocha AM, Techtmann SM (2013) Advances in monitoring environmental microbes. Curr Opin Biotech 24:526–533. doi:10.1016/J.Copbio.2012.10.020
Hazen TC, Dubinsky EA, DeSantis TZ, Andersen GL, Piceno YM, Singh N, Jansson JK, Probst A, Borglin SE, Fortney JL, Stringfellow WT, Bill M, Conrad ME, Tom LM, Chavarria KL, Alusi TR, Lamendella R, Joyner DC, Spier C, Baelum J, Auer M, Zemla ML, Chakraborty R, Sonnenthal EL, D’haeseleer P, Holman HYN, Osman S, Lu ZM, Van Nostrand JD, Deng Y, Zhou JZ, Mason OU (2010) Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330:204–208. doi:10.1126/Science.1195979
Smith MB, Rocha AM, Smillie CS, Olesen SW, Paradis C, Wu LY, Campbell JH, Fortney JL, Mehlhorn TL, Lowe KA, Earles JE, Phillips J, Techtmann SM, Joyner DC, Elias DA, Bailey KL, Hurt RA, Preheim SP, Sanders MC, Yang J, Mueller MA, Brooks S, Watson DB, Zhang P, He ZL, Dubinsky EA, Adams PD, Arkin AP, Fields MW, Zhou JZ, Alm EJ, Hazen TC (2015) Natural bacterial communities serve as quantitative geochemical biosensors. Mbio. doi:10.1128/mBio.00326-15
Shakya M, Quince C, Campbell JH, Yang ZMK, Schadt CW, Podar M (2013) Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities. Environ Microbiol 15:1882–1899. doi:10.1111/1462-2920.12086
Parada AE, Needham DM, Fuhrman JA (2015) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. doi:10.1093/nar/gks808
Prosser JI (2012) Ecosystem processes and interactions in a morass of diversity. FEMS Microbiol Ecol 81:507–519. doi:10.1111/j.1574-6941.2012.01435.x
Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu WT, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437. doi:10.1038/Nature12352
Delmont TO, Simonet P, Vogel TM (2012) Describing microbial communities and performing global comparisons in the ‘omic era. ISME J 6:1625–1628
Sharon I, Banfield JF (2013) Genomes from metagenomics. Science 342:1057–1058. doi:10.1126/science.1247023
Imelfort M, Parks D, Woodcroft BJ, Dennis P, Hugenholtz P, Tyson GW (2014) GroopM: an automated tool for the recovery of population genomes from related metagenomes. Peerj. doi:10.7717/peerj.603
Faust K, Lahti L, Gonze D, de Vos WM, Raes J (2015) Metagenomics meets time series analysis: unraveling microbial community dynamics. Curr Opin Microbiol 25:56–66. doi:10.1016/j.mib.2015.04.004
Mason OU, Scott NM, Gonzalez A, Robbins-Pianka A, Baelum J, Kimbrel J, Bouskill NJ, Prestat E, Borglin S, Joyner DC, Fortney JL, Jurelevicius D, Stringfellow WT, Alvarez-Cohen L, Hazen TC, Knight R, Gilbert JA, Jansson JK (2014) Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill. ISME J 8:1464–1475. doi:10.1038/ismej.2013.254
Moran MA, Satinsky B, Gifford SM, Luo HW, Rivers A, Chan LK, Meng J, Durham BP, Shen C, Varaljay VA, Smith CB, Yager PL, Hopkinson BM (2013) Sizing up metatranscriptomics. ISME J 7:237–243. doi:10.1038/ismej.2012.94
Vuono DC, Benecke J, Henkel J, Navidi WC, Cath TY, Munakata-Marr J, Spear JR, Drewes JE (2015) Disturbance and temporal partitioning of the activated sludge metacommunity. ISME J 9:425–435. doi:10.1038/ismej.2014.139
Zhou AF, He ZL, Qin YJ, Lu ZM, Deng Y, Tu QC, Hemme CL, Van Nostrand JD, Wu LY, Hazen TC, Arkin AP, Zhou JZ (2013) StressChip as a high-throughput tool for assessing microbial community responses to environmental stresses. Environ Sci Technol 47:9841–9849. doi:10.1021/es4018656
Hettich RL, Pan CL, Chourey K, Giannone RJ (2013) Metaproteomics: harnessing the power of high performance mass spectrometry to identify the suite of proteins that control metabolic activities in microbial communities. Anal Chem 85:4203–4214. doi:10.1021/ac303053e
Xiong WL, Abraham PE, Li Z, Pan CL, Hettich RL (2015) Microbial metaproteomics for characterizing the range of metabolic functions and activities of human gut microbiota. Proteomics 15:3424–3438. doi:10.1002/pmic.201400571
Darwin C (1859) On the origin of the species by natural selection. Murray, London
Watson DB, Kostka JE, Fields MW, Jardine PM (2004) The Oak Ridge Field Research Center conceptual model. https://public.ornl.gov/orifc/FRC-conceptual-model.pdf. Accessed 9 March 2016
Paradis CJ, Jagadamma S, Watson DB, McKay LD, Hazen TC, Park M, Istok JD (2016) In situ mobility of uranium in the presence of nitrate following sulfate-reducing conditions. J Contam Hydrol 187:55–64
Hemme CL, Tu QC, Shi Z, Qin YJ, Gao WM, Deng Y, Van Nostrand JD, Wu LY, He ZL, Chain PSG, Tringe SG, Fields MW, Rubin EM, Tiedje JM, Hazen TC, Arkin AP, Zhou JZ (2015) Comparative metagenomics reveals impact of contaminants on groundwater microbiomes. Front Microbiol. doi:10.3389/fmicb.2015.01205
Lancaster WA, Menon AL, Scott I, Poole FL, Vaccaro BJ, Thorgersen MP, Geller J, Hazen TC, Hurt RA, Brown SD, Elias DA, Adams MWW (2014) Metallomics of two microorganisms relevant to heavy metal bioremediation reveal fundamental differences in metal assimilation and utilization. Metallomics 6:1004–1013. doi:10.1039/c4mt00050a
Mohanty SR, Kollah B, Brodie EL, Hazen TC, Roden EE (2011) 16S rRNA gene microarray analysis of microbial communities in ethanol-stimulated subsurface sediment. Microbes Environ 26:261–265. doi:10.1264/jsme2.ME11111
Hemme CL, Deng Y, Gentry TJ, Fields MW, Wu LY, Barua S, Barry K, Tringe SG, Watson DB, He ZL, Hazen TC, Tiedje JM, Rubin EM, Zhou JZ (2010) Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J 4:660–672. doi:10.1038/ismej.2009.154
Istok JD, Senko JM, Krumholz LR, Watson D, Bogle MA, Peacock A, Chang YJ, White DC (2004) In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environ Sci Technol 38:468–475. doi:10.1021/es034639p
Wu WM, Carley J, Fienen M, Mehlhorn T, Lowe K, Nyman J, Luo J, Gentile ME, Rajan R, Wagner D, Hickey RF, Gu BH, Watson D, Cirpka OA, Kitanidis PK, Jardine PM, Criddle CS (2006) Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 1. Conditioning of a treatment zone. Environ Sci Technol 40:3978–3985. doi:10.1021/es051954y
Gihring TM, Zhang GX, Brandt CC, Brooks SC, Campbell JH, Carroll S, Criddle CS, Green SJ, Jardine P, Kostka JE, Lowe K, Mehlhorn TL, Overholt W, Watson DB, Yang ZM, Wu WM, Schadt CW (2011) A limited microbial consortium is responsible for extended bioreduction of uranium in a contaminated aquifer. Appl Environ Microbiol 77:5955–5965. doi:10.1128/Aem.00220-11
Fields MW, Bagwell CE, Carroll SL, Yan T, Liu X, Watson DB, Jardine PM, Criddle CS, Hazen TC, Zhou J (2006) Phylogenetic and functional biomarkers as indicators of bacterial community responses to mixed-waste contamination. Environ Sci Technol 40:2601–2607. doi:10.1021/es051748q
Kavitha S, Selvakumar R, Sathishkumar M, Swaminathan K, Lakshmanaperumalsamy P, Singh A, Jain SK (2009) Nitrate removal using Brevundimonas diminuta MTCC 8486 from ground water. Water Sci Technol 60:517–524. doi:10.2166/wst.2009.378
Green SJ, Prakash O, Jasrotia P, Overholt WA, Cardenas E, Hubbard D, Tiedje JM, Watson DB, Schadt CW, Brooks SC, Kostka JE (2012) Denitrifying bacteria from the genus Rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site. Appl Environ Microbiol 78:1039–1047. doi:10.1128/Aem.06435-11
Dubinsky EA, Conrad ME, Chakraborty R, Bill M, Borglin SE, Hollibaugh JT, Mason OU, Piceno YM, Reid FC, Stringfellow WT, Tom LM, Hazen TC, Andersen GL (2013) Succession of hydrocarbon-degrading bacteria in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ Sci Technol 47:10860–10867. doi:10.1021/es401676y
National Research Council (2005) Oil spill dispersants: efficacy and effects. The National Academies Press, Washington DC
Hazen TC, Prince RC, Mahmoudi N (2016) Marine oil biodegradation. Environ Sci Technol 50:2121–2129. doi:10.1021/acs.est.5b03333
Atlas RM, Hazen TC (2011) Oil biodegradation and bioremediation: a tale of the two worst spills in US history. Environ Sci Technol 45:6709–6715. doi:10.1021/Es2013227
King GM, Kostka JE, Hazen TC, Sobecky PA (2015) Microbial responses to the Deepwater Horizon oil spill: from coastal wetlands to the deep sea. Annu Rev Mar Sci 7:377–401. doi:10.1146/annurev-marine-010814-015543
Crone TJ, Tolstoy M (2010) Magnitude of the 2010 Gulf of Mexico oil leak. Science 330:634–636. doi:10.1126/science.1195840
Reddy CM, Arey JS, Seewald JS, Sylva SP, Lemkau KL, Nelson RK, Carmichael CA, McIntyre CP, Fenwick J, Ventura GT, Van Mooy BAS, Camilli R (2012) Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc Natl Acad Sci USA 109:20229–20234. doi:10.1073/pnas.1101242108
Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182. doi:10.1038/Nrmicro1348
Yakimov MM, Timmis KN (2007) Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotech 18:257–266. doi:10.1016/J.Copbio.2007.04.006
Camilli R, Reddy CM, Yoerger DR, Van Mooy BAS, Jakuba MV, Kinsey JC, McIntyre CP, Sylva SP, Maloney JV (2010) Tracking hydrocarbon plume transport and biodegradation at Deepwater Horizon. Science 330:201–204. doi:10.1126/science.1195223
Redmond MC, Valentine DL (2012) Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc Natl Acad Sci USA 109:20292–20297. doi:10.1073/Pnas.1108756108
Gutierrez T, Singleton DR, Berry D, Yang TT, Aitken MD, Teske A (2013) Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP. ISME J 7:2091–2104. doi:10.1038/Ismej.2013.98
Mason OU, Hazen TC, Borglin S, Chain PSG, Dubinsky EA, Fortney JL, Han J, Holman HYN, Hultman J, Lamendella R, Mackelprang R, Malfatti S, Tom LM, Tringe SG, Woyke T, Zhou JH, Rubin EM, Jansson JK (2012) Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J 6:1715–1727. doi:10.1038/Ismej.2012.59
Brugge D, Buchner V (2011) Health effects of uranium: new research findings. Rev Environ Health 26:231–249
Newsome L, Morris K, Lloyd JR (2014) The biogeochemistry and bioremediation of uranium and other priority radionuclides. Chem Geol 363:164–184
Lovley DR, Phillips EJP, Gorby YA, Landa ER (1991) Microbial reduction of uranium. Nature 350:413–416. doi:10.1038/350413a0
Williams KH, Long PE, Davis JA, Wilkins MJ, N’Guessan AL, Steefel CI, Yang L, Newcomer D, Spane FA, Kerkhof LJ, McGuinness L, Dayvault R, Lovley DR (2011) Acetate availability and its influence on sustainable bioremediation of uranium-contaminated groundwater. Geomicrobiol J 28:519–539. doi:10.1080/01490451.2010.520074
Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Long PE, Dayvault R, Karp K, Marutzky S, Metzler DR, Peacock A, White DC, Lowe M, Lovley DR (2003) Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl Environ Microbiol 69:5884–5891. doi:10.1128/Aem.69.10.5884-5891.2003
Chandler DP, Kukhtin A, Mokhiber R, Knickerbocker C, Ogles D, Rudy G, Golova J, Long P, Peacock A (2010) Monitoring microbial community structure and dynamics during in situ U(VI) bioremediation with a field-portable microarray analysis system. Environ Sci Technol 44:5516–5522. doi:10.1021/es1006498
Chang Y-J, Long PE, Geyer R, Peacock AD, Resch CT, Sublette K, Pfiffner S, Smithgall A, Anderson RT, Vrionis HA (2005) Microbial incorporation of 13C-labeled acetate at the field scale: detection of microbes responsible for reduction of U (VI). Environ Sci Technol 39:9039–9048
Kerkhof LJ, Williams KH, Long PE, McGuinness LR (2011) Phase preference by active, acetate-utilizing bacteria at the rifle, CO integrated field research challenge site. Environ Sci Technol 45:1250–1256. doi:10.1021/es102893r
Holmes DE, Giloteaux L, Barlett M, Chavan MA, Smith JA, Williams KH, Wilkins M, Long P, Lovley DR (2013) Molecular analysis of the in situ growth rates of subsurface Geobacter species. Appl Environ Microbiol 79:1646–1653. doi:10.1128/Aem.03263-12
Wilkins MJ, VerBerkmoes NC, Williams KH, Callister SJ, Mouser PJ, Elifantz H, N’Guessan AL, Thomas BC, Nicora CD, Shah MB, Abraham P, Lipton MS, Lovley DR, Hettich RL, Long PE, Banfield JF (2009) Proteogenomic monitoring of Geobacter physiology during stimulated uranium bioremediation. Appl Environ Microbiol 75:6591–6599. doi:10.1128/Aem.01064-09
Handley KM, Wrighton KC, Piceno YM, Andersen GL, DeSantis TZ, Williams KH, Wilkins MJ, N’Guessan AL, Peacock A, Bargar J, Long PE, Banfield JF (2012) High-density PhyloChip profiling of stimulated aquifer microbial communities reveals a complex response to acetate amendment. FEMS Microbiol Ecol 81:188–204. doi:10.1111/j.1574-6941.2012.01363.x
N’Guessan AL, Moon HS, Peacock AD, Tan H, Sinha M, Long PE, Jaffe PR (2010) Postbiostimulation microbial community structure changes that control the reoxidation of uranium. FEMS Microbiol Ecol 74:184–195. doi:10.1111/j.1574-6941.2010.00933.x
Liang YT, Van Nostrand JD, N’Guessan LA, Peacock AD, Deng Y, Long PE, Resch CT, Wu LY, He ZL, Li GH, Hazen TC, Lovley DR, Zhou JZ (2012) Microbial functional gene diversity with a shift of subsurface redox conditions during in situ uranium reduction. Appl Environ Microbiol 78:2966–2972. doi:10.1128/Aem.06528-11
Callister SJ, Wilkins MJ, Nicora CD, Williams KH, Banfield JF, VerBerkmoes NC, Hettich RL, N’Guessan L, Mouser PJ, Elifantz H, Smith RD, Loyley DR, Lipton MS, Long PE (2010) Analysis of biostimulated microbial communities from two field experiments reveals temporal and spatial differences in proteome profiles. Environ Sci Technol 44:8897–8903. doi:10.1021/es101029f
Waldron PJ, Wu LY, Van Nostrand JD, Schadt CW, He ZL, Watson DB, Jardine PM, Palumbo AV, Hazen TC, Zhou JZ (2009) Functional gene array-based analysis of microbial community structure in groundwaters with a gradient of contaminant levels. Environ Sci Technol 43:3529–3534. doi:10.1021/es803423p
Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-Vogel M, Kitanidis PK, Jardine PM, Zhou J, Criddle CS, Marsh TL, Tiedje JA (2008) Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl Environ Microbiol 74:3718–3729. doi:10.1128/Aem.02308-07
Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu BH, Ginder-Vogel M, Kitanidis PK, Jardine PM, Zhou JZ, Criddle CS, Marsh TL, Tiedje JM (2010) Significant association between sulfate-reducing bacteria and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach. Appl Environ Microbiol 76:6778–6786. doi:10.1128/Aem.01097-10
Borden RC, Rodriguez BX (2006) Evaluation of slow release substrates for anaerobic bioremediation. Biorem J 10:59–69
Brown SD, Utturkar SM, Magnuson TS, Ray AE, Poole FL, Lancaster WA, Thorgersen MP, Adams MW, Elias DA (2014) Complete genome sequence of Pelosinus sp. strain UFO1 assembled using single-molecule real-time DNA sequencing technology. Genome Announc 2:e00814–e00881
Ray AE, Bargar JR, Sivaswamy V, Dohnalkova AC, Fujita Y, Peyton BM, Magnuson TS (2011) Evidence for multiple modes of uranium immobilization by an anaerobic bacterium. Geochim Cosmochim Acta 75:2684–2695
Zhang P, Wu W-M, Van Nostrand JD, Deng Y, He Z, Gihring T, Zhang G, Schadt CW, Watson D, Jardine P (2015) Dynamic succession of groundwater functional microbial communities in response to emulsified vegetable oil amendment during sustained in situ U (VI) reduction. Appl Environ Microbiol 81:4164–4172
Acknowledgments
This work was in part supported by contract A13-0119-001 Deep Sea Basin Microbiology between the University of Tennessee and BP.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Techtmann, S.M., Hazen, T.C. Metagenomic applications in environmental monitoring and bioremediation. J Ind Microbiol Biotechnol 43, 1345–1354 (2016). https://doi.org/10.1007/s10295-016-1809-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10295-016-1809-8