Abstract
Microbial activity in petroleum reservoirs has been implicated in a suite of detrimental effects including deterioration of petroleum quality, increases in oil sulfur content, biofouling of steel pipelines and other infrastructures, and well plugging. Here, we present a biogeochemical approach, using phospholipid fatty acids (PLFAs), for detecting viable bacteria in petroleum systems. Variations within the bacterial community along water flow paths (producing well, topside facilities, and injection well) can be elucidated in the field using the same technique, as shown here within oil production plants in the Molasse Basin of Upper Austria. The abundance of PLFAs is compared to total cellular numbers, as detected by qPCR of the 16S rDNA gene, to give an overall comparison between the resolutions of both methods in a true field setting. Additionally, the influence of biocide applications on lipid- and DNA-based quantification was investigated. The first oil field, Trattnach, showed significant PLFA abundances and cell numbers within the reservoir and topside facilities. In contrast, the second field (Engenfeld) showed very low PLFA levels overall, likely due to continuous treatment of the topside facilities with a glutaraldehyde-based antimicrobial. In comparison, Trattnach is dosed once per week in a batch fashion. Changes within PLFA compositions across the flow path, throughout the petroleum production plants, point to cellular adaptation within the system and may be linked to shifts in the dominance of certain bacterial types in oil reservoirs versus topside facilities. Overall, PLFA-based monitoring provides a useful tool to assess the abundance and high-level taxonomic diversity of viable microbial populations in oil production wells, topside infrastructure, pipelines, and other related facilities.
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References
Head IM, Jones DM, Larter SR (2003) Biological activity in the deep subsurface and the origin of heavy oils. Nature 426:344–352. doi:10.1038/nature02134
Beech IB, Sunner J (2004) Biocorrosion: towards understanding interactions between biofilms and metals. Curr. Opin. Biotechnol. 15:181–186
McInerney MJ, Sublette KL (eds) (1997) Petroleum microbiology: biofouling, souring, and improved oil recovery. ASM Press, Washington DC
Magot M, Ollivier G, Patel GKC (2000) Microbiology of petroleum reservoirs. Anton. Leeuw. Int. J. Gen. Mol. Microbiol. 77:103–116. doi:10.1023/A:1002434330514
Van Nostrand JD, He Z, Zhou J (2010) Analysis of microbial communities by functional gene arrays. In: Barton LL, Mandl M, Loy A (eds) Geomicrobiology: molecular and environmental perspective. Springer, Dordrecht
Grabowski A, Nercessian O, Fayolle F, Blanchet D, Jeanthon C (2005) Microbial diversity in production waters of a low-temperature biodegraded oil reservoir. FEMS Microbiol. Ecol. 54:427–443. doi:10.1016/j.resmic.2005.03.009
Connan J, Lacrampe-Coulombe G, Magot M (1996) Origin of gases in reservoirs. International Gas Research Conference, Government Institutes, Rockville, pp. 21–61
Röling WFM, Head IM, Larter SR (2003) The microbiology of hydrocarbon degradation in subsurface petroleum reservoirs: perspectives and prospects. Res. Microbiol. 154:321–328. doi:10.1016/S0923-2508(03)00086-X
Hallmann C, Schwark L, Grice K (2008) Community dynamics of anaerobic bacteria in deep petroleum reservoirs. Nat. Geosci. 1:588–591. doi:10.1038/ngeo260
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: a review. Biol Fert Soils 29:111–129. doi:10.1007/s003740050533
Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. FEMS Microbiol. Ecol. 35:265–278. doi:10.1007/s002489900082
Green CT, Scow KM (2000) Analysis of phospholipid fatty acids (PLFA) to characterize microbial communities in aquifers. Hydrogeol. J. 8:126–141. doi:10.1007/s100400050013
White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62. doi:10.1007/BF00388810
Schubotz F, Lipp JS, Elvert M, Kasten S, Mollar XP, Zabel M, Bohrmann G, Hinrichs K-U (2011) Petroleum degradation and associated microbial signatures at the Chapopote asphalt volcano, Southern Gulf of Mexico. Geochim Cosmochim Ac 75:4377–4398. doi:10.1016/j.gca.2011.05.025
Harvey HR, Fallon RD, Patton JS (1986) The effect of organic matter and oxygen on the degradation of bacterial membrane lipids in marine sediments. Geochim Cosmochim Ac 50:795–804. doi:10.1016/0016-7037(86)90355-8
Petsch ST, Edwards KJ, Eglinton TI (2003) Abundance, distribution and δ13C analysis of microbial phospholipid-derived fatty acids in a black shale weathering profile. Org. Geochem. 34:731–743. doi:10.1016/S0146-6380(03)00040-8
Vetter A, Mangelsdorf K, Wolfgramm M, Rauppach K, Schettler G, Vieth-Hillebrand A (2012) Variations in fluid chemistry and membrane phospholipid fatty acid composition of the bacterial community in a cold storage ground water system during clogging events. Appl. Geochem. 27:1278–1290. doi:10.1016/j.apgeochem.2012.02.022
Vetter A, Mangelsdorf K, Schettler G, Seibt A, Wolfgramm M, Rauppach K, Vieth-Hillebrand A (2012) Fluid chemistry and impact of different operating modes on microbial community at Neubrandenburg heat storage (Northeast German Basin). Org. Geochem. 53:8–15. doi:10.1016/j.orggeochem.2012.08.008
Oldenburg TBP, Larter SR, Adams JJ, Clements M, Hubert C, Rowan AK, Brown A, Head IM, Grigoriyan AA, Voordouw G, Fustic M (2009) Methods for recovery of microorganisms and intact microbial polar lipids from oil-water mixtures: laboratory experiments and natural well-head fluids. Anal. Chem. 81:4130–4136. doi:10.1021/ac8025515
Vestal JR, White DD (1989) Lipid analysis in microbial ecology—quantitative approaches to the study of microbial communities. Bioscience 39:535–541
Summit M, Peacock A, Ringelberg D, White DC, Baross JA (2000) Phospholipid fatty acid-derived microbial biomass and community dynamics in hot, hydrothermally influenced sediments from Middle Valley, Juan de Fuca Ridge. Proceedings of the Ocean Drilling Program, Scientific Results Volume 169: Chapter 3
Aries E, Doumenq P, Artaud J, Molinet J, Bertrand JC (2001) Occurrence of fatty acids linked to non-phospholipid compounds in the polar fraction of a marine sedimentary extract from Carteau cove, France. Org. Geochem. 32:193–197. doi:10.1016/S0146-6380(00)00153-4
Chang Y-J, Peacock AD, Long PE, Stephen JR, McKinley JP, MacNaughton SJ, Hussain AKMA, Saxton AM, White DC (2001) Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailing site. Appl Environ Microb 67:3149–3160. doi:10.1128/AEM.67.7.3149-3160.2001
Pratt B, Riesen R, Johnston CG (2012) PLFA analyses of microbial communities associated with PAH-contaminated riverbank sediment. Environ. Microbiol. 64:680–691. doi:10.1007/s00248-012-0060-8
Li Y-L, Peacock AD, White DC, Geyer R, Zhang CL (2007) Spatial patterns of bacterial signature biomarkers in marine sediments of the Gulf of Mexico. Chem. Geol. 238:168–179. doi:10.1016/j.chemgeo.2006.11.007
Dowling NJE, Widdel F, White DC (1986) Phospholipid ester-linked fatty acid biomarkers of acetate-oxidizing sulfate-reducers and other sulfide-forming bacteria. J. Gen. Microbiol. 132:1815–1825. doi:10.1099/00221287-132-7-1815
Sikkema J, De Bond JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59:201–222
Guckert JB, Hood MA, White DC (1986) Phospholipid ester-linked fatty acid profile changes during nutrient deprivation of Vibrio cholera: increases in the cis/trans ratio and proportions of cyclopropyl fatty acids. Appl Environ Microb 52:794–801
Haubert D, Häggblom MM, Scheu S, Ruess L (2008) Effects of temperature and life stage on the fatty acid composition of Collembola. Eur J Soil Biol 44:213–219. doi:10.1016/j.ejsobi.2007.09.003
Hazel JR, Williams EE (1991) The role of alterations in membrane lipid composition in enabling physiological adaptation in organisms to their physical environment. Prog. Lipid Res. 29:167–227. doi:10.1016/0163-7827(90)90002-3
Petersen SO, Klug MJ (1994) Effects of sieving, storage and incubation temperature on the phospholipid fatty acid profile of a soil microbial community. Appl Environ Microb 60:2421–2430
Sachsenhofer RF, Gratzer R, Tschelaut W, Bechtel A (2006) Characterization of non-producible oil in Eocene reservoirs sandstones (Bad Hall Nord field, Alpine Foreland Basin, Austria). Mar Petrol Geol 23:1–15. doi:10.1016/j.marpetgeo.2005.07.002
Hamilton W, Wagner L, Wessely G (1999) Oil and gas in Austria. Mitt. Österr. Geol. Ges. 92:235–262
Gratzer R, Bechtel A, Sachsenhofer RF, Linzer H-G, Reischenbacher D, Schulz H-M (2011) Oil-oil and oil-source correlations in the Alpine Foreland Basin of Austria: insights from biomarker and stable carbon isotope studies. Mar Petrol Geol 28:1171–1186. doi:10.1016/j.marpetgeo.2011.03.001
Bechtel A, Gratzer R, Linzer H-G, Sachsenhofer RF (2013) Influence of migration distance, maturity and facies of the stable isotopic composition of alkanes and on carbazole distributions in oils and source rocks of the Alpine Foreland basin of Austria. Org. Geochem. 62:74–85. doi:10.1016/j.orggeochem.2013.07.008
Reischenbacher D, Sachsenhofer RF (2011) Entstehung von Erdgas in der oberösterreichischen Molassezone: Daten und offene Fragen. Berg- und Hüttenmännische Monatshefte 156:455–460. doi:10.1007/s00501-011-0037-9
Andrews JN, Youngman MJ, Goldbrunner JE, Darling WG (1987) The geochemistry of formation waters in the Molasse Basin of Upper Austria. Environ Geol Water S 10:43–57. doi:10.1007/BF02588004
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917. doi:10.1139/o59-099
Zink K-G, Mangelsdorf K (2004) Efficient and rapid method for extraction of intact phospholipids from sediments combined with molecular structure elucidation using LC-ESI-MS-MS analysis. Anal. Bioanal. Chem. 380:798–812. doi:10.1007/s00216-004-2828-2
Müller K-D, Husmann H, Nalik HP (1990) A new and rapid method for the assay of bacterial fatty acids using high resolution capillary gas chromatography and trimethylsulfonium hydroxide. Zbl Bakt 274:174–182. doi:10.1016/S0934-8840(11)80100-3
Jiang Y, Marang L, Kleerebezem R, Muyzer G, van Loosdrecht MCM (2011) Effect of temperature and cycle length on microbial competition in PHB-producing sequencing batch reactor. ISME J 5:896–907
Vroblesky DA, Bradley PM, Chapelle FH (1996) Influence of electron donor on the minimum sulfate concentration required for sulfate reduction in a petroleum hydrocarbon-contaminated aquifer. Environ Sci Technol 30:1377–1381. doi:10.1021/es950684o
Sinninghe Damsté JS, Rijpstra WIC, Hopmans EC, Schouten S, Balk M, Stams AJM (2007) Structural characterization of diabolic acid-based tetraester, tetraether and mixed ether/ester, membrane-spanning lipids of bacteria from the order Thermotogales. Arch. Microbiol. 188:629–641. doi:10.1007/s00203-007-0284-z
Huber R, Hannig M (2005) Thermotogales. In: Dworkin M et al. (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer, New York
Dahle H, Garshol F, Madsen M, Birkeland N-K (2007) Microbial community structure analysis of produced water from a high-temperature North Sea oil-field. Anton Leeuw 93:37–49. doi:10.1007/s10482-007-9177-z
Agrawal A, An D, Cavallaro A, Voordouw G (2014) Souring in low-temperature surface facilities of two high-temperature Argentinian oil fields. Appl Microbiol Biotechnol 98:8017–8029. doi:10.1007/s00253-014-5843-z
Lipp JS, Hinrichs K-U (2009) Structural diversity and fate of intact polar lipids in marine sediments. Geochim Cosmochim Ac 73:6816–6833. doi:10.1016/j.gca.2009.08.003
Coleman ML, Hedrick DB, Lovley DR, White DC, Pye K (1993) Reduction of Fe(III) in sediments by sulfate reducing bacteria. Nature 361:436–438. doi:10.1038/361436a0
Smith CA, Phiefer CB, MacNaughton SJ, Peacock A, Burkhalter RS, Kirkegaard R, White DC (2000) Quantitative lipid biomarker detection of unculturable microbes and chlorine exposure in water distribution system biofilms. Water Res. 34:2683–2688. doi:10.1016/S0043-1354(00)00028-2
Collins MD, Keddie RM, Kroppenstedt RM (1983) Lipid composition of Arthrobacter simplex, Arthrobacter tumescens, and possibly related taxa. Syst Appl Microbiol 4:18–26. doi:10.1016/S0723-2020(83)80030-7
White DC, Stair JO, Ringelberg DB (1996) Quantitative comparisons of in situ microbial diversity by signature biomarker analysis. J. Ind. Microbiol. 17:185–196
Klamer M, Bååth E (1998) Microbial community dynamics during composting of straw material studied using phospholipid fatty acid analysis. FEMS Microbiol. Ecol. 27:9–20. doi:10.1111/j.1574-6941.1998.tb00521.x 9-20
Russell NJ (1989) Functions of lipids: structural roles and membrane functions. In: Radledge C, Wilkinson SG (eds) Microbial Lipids 2. Academic Press, London, pp. 279–365
Acknowledgements
This research project was supported by funding from Dow Microbial Control. We are grateful for the excellent collaboration with Rohöl-Aufsuchungs Aktiengesellschaft (RAG) and the University of Leoben. We thank two anonymous reviewers for their constructive comments which helped to improve the manuscript. We would also like to kindly acknowledge technical support provided by Kristin Guenther, Cornelia Karger, and Maria Bade at the GFZ and Imke Widera at Dow Europe GmbH.
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Gruner, A., Mangelsdorf, K., Vieth-Hillebrand, A. et al. Membrane Lipids as Indicators for Viable Bacterial Communities Inhabiting Petroleum Systems. Microb Ecol 74, 373–383 (2017). https://doi.org/10.1007/s00248-017-0954-6
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DOI: https://doi.org/10.1007/s00248-017-0954-6