Restricted accessResearch articleFirst published online 2016-10
Comparative Study of Effects of CO 2 Concentration and pH on Microbial Communities from a Saline Aquifer,a Depleted Oil Reservoir,and a Freshwater Aquifer
Injected CO2 from geologic carbon storage is expected to impact the microbial communities of proposed storage sites, such as depleted oil reservoirs and deep saline aquifers, as well as overlying freshwater aquifers at risk of receiving leaking CO2. Microbial community change in these subsurface sites may affect injectivity of CO2, permanence of stored CO2, and shallow subsurface water quality. The effect of CO2 concentration on the microbial communities in fluid collected from a depleted oil reservoir and a freshwater aquifer was examined at subsurface pressures and temperatures. The community was exposed to 0%, 1%, 10%, and 100% pCO2 for 56 days. Bacterial community structure was analyzed through 16S rRNA gene clone libraries, and total bacterial abundance was estimated through quantitative polymerase chain reaction. Changes in the microbial community observed in the depleted oil reservoir samples and freshwater samples were compared to previous results from CO2-exposed deep saline aquifer fluids. Overall, results suggest that CO2 exposure to microbial communities will result in pH-dependent population change, and the CO2-selected microbial communities will vary among sites. This is the first study to compare the response of multiple subsurface microbial communities at conditions expected during geologic carbon storage, increasing the understanding of environmental drivers for microbial community changes in CO2-exposed environments.
Get full access to this article
View all access options for this article.
References
1.
AllenD.A., AustinB., and ColwellR.R. (1977). Antibiotic-resistance patterns of metal-tolerant bacteria isolated from an estuary. Antimicrob. Agents Chemother., 12, 545.
2.
AltschulS.F., GishW., MillerW., MyersE.W., and LipmanD.J. (1990). Basic local alignment search tools. J. Mol. Biol., 215, 403.
3.
AmannR.I., LudwigW., and SchleiferK.H. (1995). Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation. Microbiol. Rev., 59, 143.
4.
AmendJ.P., and TeskeA. (2005). Expanding frontiers in deep subsurface microbiology. Palaeogeogr. Palaeocl., 219, 131.
5.
BensonS.M., AppsJ., HeppleR., LippmannM., TsangC.F., and LewisC. (2003). Health, safety and environmental risk assessment for geologic storage of carbon dioxide: Lessons learned from industrial and natural analogues. Presented at the 6th International Conference on Greenhouse Gas Control Technologies, Kyoto, Japan, September 30–October 4.
6.
BergmoP.E.S., GrimstadA.A., and LindebergE. (2011). Simultaneous CO2 injection and water production to optimise aquifer storage capacity. Int. J. Greenhouse Gas Control, 5, 555.
7.
BernardetJ.F., NakagawaY., HolmesB; Subcommittee on the taxonomy of Flavobacterium and Cytophaga-like bacteria of the International Committee on Systematics of Prokaryotes. (2002). Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emended description of the family. Int. J. Syst. Evol. Microbiol., 52, 1049.
8.
BinL., YeC., LijunZ., and RuidongY. (2008). Effect of microbial weathering on carbonate rocks. Front Earth Sci. 15, 90.
9.
CeliaM.A., and BachuS. (2003). Geological sequestration of CO2: Is leakage unavoidable and acceptable?Presented at the 6th International Conference on Greenhouse Gas Control Technologies, Kyoto, Japan, September 30–October 4.
10.
CunninghamA.B., GerlachR., SpanglerL., and MitchellA.C. (2009). Microbially enhanced geologic containment of sequestered supercritical CO2. Energy Procedia. 1, 3245.
11.
DafflonB., WuY.X., HubbardS.S., BirkholzerJ.T., DaleyT.M., PughJ.D., PetersonJ.E., and TrautzR.C. (2013). Monitoring CO2 intrusion and associated geochemical transformations in a shallow groundwater system using complex electrical methods. Environ. Sci. Technol., 47, 314.
12.
DekkerL., OsborneT.H., and SantiniJ.M. (2014). Isolation and identification of cobalt and caesium resistant bacteria from a nuclear fuel storage pond. FEMS Microbiol. Lett., 359, 81.
13.
DelongE.F. (1992). Archaea in coastal marine environments. Proc. Natl. Acad. Sci., 89, 5685.
14.
DillowA.K., DehghaniF., HrkachJ.S., FosterN.R., and LangerR. (1999). Bacterial inactivation by using near- and supercritical carbon dioxide. Proc. Natl. Acad. Sci., 96, 10344.
15.
DingL.X., and YokotaA. (2004). Proposals of Curvibacter gracilis gen. nov., sp nov and Herbaspirillum putei sp nov for bacterial strains isolated from well water and reclassification of Pseudomonas huttiensis, Pseudomonas lanceolata, Aquaspirillum delicatum and Aquaspirillum autotrophicum as Herbaspirillum huttiense comb. nov., Curvibacter lanceolatus comb. nov., Curvibacter delicatus comb. nov and Herbaspirillum autotrophicum comb. nov. Int. J. Syst. Evol. Microbiol., 54, 2223.
16.
Falcone-DiasM.F., Vaz-MoreiraI., and ManaiaC.M. (2012). Bottled mineral water as a potential source of antibiotic resistant bacteria. Water Res. 46, 3612.
17.
Fernandez-CalvinoD., and BaathE. (2010). Growth response of the bacterial community to pH in soils differing in pH. FEMS Microbiol. Ecol., 73, 149.
18.
FitzgeraldL.A., PetersenE.R., GrossB.J., SotoC.M., RingeisenB.R., El-NaggarM.Y., and BiffingerJ.C. (2012). Aggrandizing power output from Shewanella oneidensis MR-1 microbial fuel cells using calcium chloride. Biosens. Bioelectron., 31, 492.
19.
FrerichsJ., RakoczyJ., Ostertag-HenningC., and KruegerM. (2014). Viability and adaptation potential of indigenous microorganisms from natural gas field fluids in high pressure incubations with supercritical CO2. Environ. Sci. Technol., 48, 1306.
20.
GaddG.M. (2004). Microbial influence on metal mobility and application for bioremediation. Geoderma, 122, 109.
21.
GillC.O., and TanK.H. (1979). Effect of carbon dioxide on the growth of Pseudomonas-fluorescens. Appl. Environ. Microbiol., 38, 237.
22.
GulliverD.M., LowryG.V., and GregoryK.B. (2014). CO2 concentration and pH alters subsurface microbial ecology at reservoir temperature and pressure. RSC Adv. 4, 17443.
23.
GulliverD.M., LowryG.V., and GregoryK.B. (2014). Effect of CO2(aq) exposure on a freshwater aquifer microbial community from simulated geologic carbon storage leakage. Environ. Sci. Technol., 1, 479.
24.
HamamuraN., FukushimaK., and ItaiT. (2013). Identification of antimony- and arsenic-oxidizing bacteria associated with antimonay mine tailing. Microbes Environ. 28, 257.
25.
HammesF., and VerstraeteW. (2002). Key roles of pH and calcium metabolism in microbial carbonate precipitation. Rev. Environ. Sci. Biotechnol., 1, 3.
26.
HolmesD.E., BondD.R., and LovleyD.R. (2004). Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl. Environ. Microbiol., 70, 1234.
27.
HuberT., FaulknerG., and HugenholtzP. (2004). Bellerophon: A program to detect chimeric sequences in multiple sequence alignments. Bioinformatics, 20, 2317.
28.
IshiiS., and SadowskyM.J. (2008). Escherichia coli in the environment: Implications for water quality and human health. Microbes Environ. 23, 101.
29.
KazubaJ.P., JanekyD.R., and SnowM.G. (2003). Carbon dioxide reaction processes in a model brine aquifer at 200°C and 200 bar: Implications for geologic sequestration of carbon. Appl. Geochem., 18, 1065.
30.
KharakaY.K., ThordsenJ.J., HovorkaS.D., NanceH.S., ColeD.R., PhelpsT.J., and KnaussK.G. (2009). Potential environmental issues of CO2 storage in deep saline aquifers: Geochemical results from the Frio-I Brine Pilot test, Texas.
31.
KutchkoB.G., StrazisarB.R., DzombakD.A., LowryG.V., and ThaulowN. (2007). Degradation of well cement by CO2 under geologic sequestration conditions. Environ. Sci. Technol., 41, 4787.
32.
LalucatJ., BennasarA., BoschR., Garcia-ValdesE., and PalleroniN.J. (2006). Biology of Pseudomonas stutzeri. Microbiol. Mol. Biol. Rev., 70, 510.
LaneD. (1991). 16S/23S rRNA sequencing. In: StackebrandtE., and GoodfellowM., eds. Nucleic Acid Techniques in Bacterial Systematics. Chichester, England: Wiley & Sons, p. 115.
35.
LaneD., PaceB., OlsenG.J., StahlD.A., SoginM.L., and PaceN.R. (1985). Rapid determination of 16S ribisomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci., 82, 6955.
36.
LavalleurH.J., and ColwellF.S. (2013). Microbial characterization of basalt formation waters targeted for geological carbon sequestration. FEMS Microbiol. Ecol., 85, 62.
37.
LegendreP., and LegendreL. (2012). Numerical Ecology—Developments in Environmental Modeling. Oxford, UK: Elsevier.
38.
LindahlT. (1993). Instability and decay of the primary structure of DNA. Nature, 362, 709.
39.
LittleM.G., and JacksonR.B. (2010). Potential impacts of leakage from deep CO2 geosequestration on overlying freshwater aquifers. Environ. Sci. Technol., 44, 9225.
40.
LozuponeC., LladserM.E., KnightsD., StombaughJ., and KnightR. (2011). UniFrac: An effective distance metric for microbial community comparison. ISME J. 5, 169.
41.
MagotM., OllivierB., and PatelB.K.C. (2000). Microbiology of petroleum reservoirs. Antonie van Leeuwenhoek, 77, 103.
42.
MolinG. (1983). The resistance to carbon-dioxide of some food related bacteria. Eur. J. Appl. Microbiol., 18, 214.
43.
MollerB., OssmerR., HowardB.H., GottschalkG., and HippeH. (1984). Sporomusa, a new genus of gram-negative anaerobic bacteria including sporomusa-sphaeroides spec-nov and sporomusa-ovata spec-nov. Arch. Microbiol., 139, 388.
44.
National Petroleum Council (2011). Management of produced water from oil and gas. NPC North American Resource Development Study.
45.
Nguyen-HieuT., AboudharamG., and DrancourtM. (2012). Heat degradation of eukaryotic and bacterial DNA: An experimental model for paleomicrobiology. BMC Res. Notes, 5, 528.
46.
O'MullanG., DuekerM.E., ClausonK., YangQ., UmemotoK., and ZakharovaN. (2015). Microbial stimulation and succession following a test well injection simulating CO2 leakage into a shallow newark basin aquifer. PLoS One, 10, e0117812.
47.
OrdonezO.F., FloresM.R., DibJ.R., PazA., and FariasM.E. (2009). Extremophile culture collection from Andean Lakes: Extreme pristine environments that host a wide diversity of microorganisms with tolerance to UV radiation. Microb. Ecol., 58, 461.
48.
Paredes-SabjaD., SetlowP., and SarkerM.R. (2011). Germination of spores of Bacillales and Clostridiales species: Mechanisms and proteins involved. Trends Microbiol. 19, 85.
49.
ParkJ., SanfordR.A., and BethkeC.M. (2009). Microbial activity and chemical weathering in the Middendorf aquifer, South Carolina. Chem. Geol., 258, 232.
50.
PeixA., Ramirez-BahenaM.H., and VelazquezE. (2009). Historical evolution and current status of the taxonomy of genus Pseudomonas. Infect. Genet. Evol., 9, 1132.
51.
RaskinL., StromleyJ.M., RittmanB.E., and StahlD.A. (1994). Group-specific 16S ribosomal RNA hybidization probes to describe natural communities of methanogens. Appl. Environ. Microbiol., 60, 1232.
52.
RivadeneyraM.A., DelgadoR., ParragaJ., Ramos-CormenzanaA., and DelgadoG. (2006). Precipitation of minerals by 22 species of moderately halophilic bacteria in artificial marine salts media: Influence of salt concentration. Folia Microbiol. 51, 445.
53.
Sanchez-RomanM., RivadeneyraM.A., VasconcelosC., and McKenzieJ.A. (2007). Biomineralization of carbonate and phosphate by moderately halophilic bacteria. FEMS Microbiol. Ecol., 61, 273.
54.
SatputeS.K., BanatI.M., DhakephalkarP.K., BanpurkarA.G., and ChopadeB.A. (2010). Biosurfactants, bioemulsifiers, and exopolysaccharides from marine microorganisms. Biotechnol. Adv., 28, 436.
55.
SchlossP.D., WestcottS.L., RyabinT., HallJ.R., HartmannM., HollisterE.B., LesniewskiR.A., OakleyB.B., ParksD.H., RobinsonC.J., SahlJ.W., StresB., ThallingerG.G., Van HornD.J., and WeberC.F. (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol., 75, 7537.
56.
SchulzA., VogtC., and RichnowH.H. (2012). Effects of high CO2 concentrations on ecophysiologically different microorganisms. Environ. Pollut., 169, 27.
57.
ShahA.H., SalehaA.A., ZunitaZ., CheahY.K., MurugaiyahM., and KorejoN.A. (2012). Genetic characterization of Arcobacter isolates from various sources. Vet. Microbiol., 160, 355.
58.
SmythR.C., HovorkaS.D., LuJ., RomanakK.D., PartinJ.W., WongC., and YangC. (2009). Assessing risk of fresh water resources from long term CO2 injection-laboratory and field studies. Energy Procedia. 1, 1957.
59.
StandingM.B., and KatzD.L. (1941). Density of natural gases. Pet. Technol., 1323, 140.
60.
SuzukiM.T., TaylorL.T., and DeLongE.F. (2000). Quantitative analysis of small subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl. Environ. Microbiol., 66, 4605.
61.
Team, R.D.C. (2008). A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
62.
TrautzR.C., PughJ.D., VaradharajanC., ZhengL.G., BianchiM., NicoP.S., SpycherN.F., NewellD.L., EspositoR.A., WuY.X., DafflonB., HubbardS.S., and BirkholzerJ.T. (2013). Effect of dissolved CO2 on a shallow groundwater system: A controlled release field experiment. Environ. Sci. Technol., 47, 298.
63.
WandreyM., FischerS., ZemkeK., LiebscherA., ScherfA.K., Vieth-HillebrandA., ZettlitzerM., and WurdemannH. (2011). Monitoring petrophysical, mineralogical, geochemical and microbiological effects of CO2 exposure—Results of long-term experiments under in situ conditions. Energy Procedia. 4, 3644.
64.
WandreyM., PellizariL., ZettlitzerM., and WurdemannH. (2011). Microbial community and inorganic fluid analysis during CO2 storage within the frame of CO2SINK—Long-term experiments under in situ conditions. Energy Procedia. 4, 3651.
65.
WarscheidT., and BraamsJ. (2000). Biodeterioration of stone: A review. Int. Biodeter. Biodegr., 46, 343.
66.
WilkinsM.J., HoytD.W., MarshallM.J., AldersonP.A., PlymaleA.E., MarkillieL.M., TuckerA.E., WalterE.D., LinggiB.E., DohnalkovaA.C., and TaylorR.C. (2014). CO2 exposure at pressure impacts metabolism and stress responses in the model sulfate-reducing bacterium Desulfovibrio vulgaris strain Hildenborough. Front Microbiol. 5, 10.
67.
WuB., ShaoH.B., WangZ.P., HuY.D., TangY.J.J., and JunY.S. (2010). Viability and metal reduction of Shewanella oneidensis MR-1 under CO2 stress: Implications for ecological effects of CO2 leakage from geologic CO2 sequestration. Environ. Sci. Technol., 44, 9213.
68.
ZhangJ., DavisT., MatthewsM., DrewsM., LaBergeM., and AnY. (2006). Sterilization using high-pressure carbon dioxide. J. Supercrit. Fluid., 38, 354.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
