Skip to main content
SpringerLink
Log in

Biofilm formation and potential for iron cycling in serpentinization-influenced groundwater of the Zambales and Coast Range ophiolites

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Terrestrial serpentinizing systems harbor microbial subsurface life. Passive or active microbially mediated iron transformations at alkaline conditions in deep biosphere serpentinizing ecosystems are understudied. We explore these processes in the Zambales (Philippines) and Coast Range (CA, USA) ophiolites, and associated surface ecosystems by probing the relevance of samples acquired at the surface to in situ, subsurface ecosystems, and the nature of microbe–mineral associations in the subsurface. In this pilot study, we use microcosm experiments and batch culturing directed at iron redox transformations to confirm thermodynamically based predictions that iron transformations may be important in subsurface serpentinizing ecosystems. Biofilms formed on rock cores from the Zambales ophiolite on surface and in-pit associations, confirming that organisms from serpentinizing systems can form biofilms in subsurface environments. Analysis by XPS and FTIR confirmed that enrichment culturing utilizing ferric iron growth substrates produced reduced, magnetic solids containing siderite, spinels, and FeO minerals. Microcosms and enrichment cultures supported organisms whose near relatives participate in iron redox transformations. Further, a potential ‘principal’ microbial community common to solid samples in serpentinizing systems was identified. These results indicate collectively that iron redox transformations should be more thoroughly and universally considered when assessing the function of terrestrial subsurface ecosystems driven by serpentinization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  • Abrajano TA, Sturchio NC, Bohlke JK, Lyon GL, Poreda RJ, Stevens CM (1988) Methane–hydrogen gas seeps, Zambales ophiolite, Philippines: deep or shallow origin? Chem Geol 71:211–222

    Article  CAS  Google Scholar 

  • Arcilla CA, Pascua CS, Alexander WR (2011) Hyperalkaline groundwaters and tectonism in the Philippines: significance to natural carbon capture and sequestration. Energy Procedia 4:5093–5101

    Article  CAS  Google Scholar 

  • Barnes I, Rapp JB, O’Neill JR, Sheppard RA, Gude AJ (1972) Metamorphic assemblages and the direction of flow of metamorphic fluids in four instances of serpentinization. Contrib Mineral Petrol 35:263–276

    Article  CAS  Google Scholar 

  • Brazelton WJ (2010) Ecology of archaeal and bacterial biofilm communities at the Lost City hydrothermal field. University of Washington, Seattle

    Google Scholar 

  • Brazelton WJ, Nelson B, Schrenk MO (2012) Metagenomic evidence for H2 oxidation and H2 production by serpentine-hosted subsurface microbial communities. Front Microbiol 2:268

    Article  PubMed  PubMed Central  Google Scholar 

  • Brazelton WJ, Morrill PL, Szponar N, Schrenk MO (2013) Bacterial communities associated with subsurface geochemical processes in continental serpentinite springs. Appl Environ Microbiol 79:3906–3916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010a) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010b) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. https://doi.org/10.1093/bioinformatics/btp636

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardace D, Meyer-Dombard DR, Arcilla C, Hoehler T, McCollom T, Schrenk M (2013) Microbial metabolic landscapes derived from complementary mineralogical, aqueous geochemical, and gas data associated with high pH, actively serpentinizing springs in the Coast Range ophiolite (CA, USA) and Zambales and Palawan ophiolites (Philippines). Abstract B13C-0503 presented at 2013 Fall Meeting, AGU, San Francisco, Calif., 9–13 Dec

  • Cardace D, Meyer-Dombard DR, Woycheese KM, Arcilla C (2015) Feasible metabolisms in high pH springs in the Philippines. Front Extreme Microbiol 6:1–16

    Google Scholar 

  • Chakraborty A, Picardal F (2013) Neutrophilic, nitrate-dependent, Fe(II) oxidation by a Dechloromonas species. World J Microbiol Biotechnol 29:617–623

    Article  CAS  PubMed  Google Scholar 

  • Chan CS, De Stasio G, Welch SA, Girasole M, Frazer BH, Nesterrova MV, Fakra S, Banfield JF (2004) Microbial polysaccharides template assembly of nanocrystal fibers. Science 303:1656–1658

    Article  CAS  PubMed  Google Scholar 

  • Charlou JL, Donval JP, Konn C, Ondréas H, Fouquet Y, Jean-Baptiste P, Fourré E (2010) High production and fluxes of H2 and CH4 and evidence of abiotic hydrocarbon synthesis by serpentinization in ultramafic-hosted hydrothermal systems on the Mid-Atlantic Ridge. In: Rona PA, Devey CW, Dyment J, Murton BJ (eds) Diversity of hydrothermal systems on slow spreading ocean ridges. American Geophysical Union, Washington DC

    Google Scholar 

  • Chivian D, Brodie EL, Alm EJ, Culle DE, Dehal PS, DeSantis TZ, Gihring TM, Lapidus A, Lin L, Lowry SR, Moser DP, Richardson PM, Southam G, Wanger G, Pratt LM, Andersen GL, Hazen TC, Brockman FJ, Arkin AP, Onstott TC (2008) Environmental genomics reveals a single-species ecosystem deep within Earth. Science 322:275–278

    Article  CAS  PubMed  Google Scholar 

  • Crespo-Medina M, Twing KI, Kubo MDY, Hoehler TM, Cardace D, McCollom T, Schrenk MO (2014) Insights into environmental controls on microbial communities in a continental serpentinite aquifer using a microcosm-based approach. Front Microbiol 5:604

    Article  PubMed  PubMed Central  Google Scholar 

  • Daae FL, Økland I, Dahle H, Jørgensen SL, Thorseth IH, Pedersen RB (2013) Microbial life associated with low-temperature alteration of ultramafic rocks in the Leka ophiolite complex. Geobiology 11:318–339

    Article  CAS  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. https://doi.org/10.1128/AEM.03006-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dilek Y (2003) Ophiolite concept and its evolution. In: Dilek Y, Newcomb S (eds) Ophiolite concept and the evolution of geological thought, vol 373. Geological Society of America, Colorado, pp 1–16 (Special Papers)

    Chapter  Google Scholar 

  • Ding L-J, An X-L, Li S, Zhange G-L, Zhu Y-G (2014) Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environ Sci Technol 48:10641–10647

    Article  CAS  PubMed  Google Scholar 

  • Dobbin PS, Carter JP, San Juan CGS, von Hobe M, Powell AK, Richardson DJ (1999) Dissimilatory Fe(III) reduction by Clostridium beijerinckii isolated from freshwater sediment using Fe(III) maltol enrichment. FEMS Microbiol Lett 176:131–138

    Article  CAS  PubMed  Google Scholar 

  • Dong H, Fredrickson JK, Kennedy DW, Zachara JM, Kukkadapu RK, Onstott TC (2000) Mineral transformations associated with the microbial reduction of magnetite. Chem Geol 169:299–318

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Emerson D (2012) Biochemistry and microbiology of microaerobic Fe(II) oxidation. Biochem Soc Trans 40:1211–1216

    Article  CAS  PubMed  Google Scholar 

  • Fortin D, Langley S (2005) Formation and occurrence of biogenic iron-rich minerals. Earth Sci Rev 72:1–19

    Article  CAS  Google Scholar 

  • Fuller SJ, Burke IT, McMillan DGG, Ding W, Stewart DI (2015) Population changes in a community of alkaliphilic iron-reducing bacteria due to changes in the electron acceptor: implications for bioremediation at alkaline Cr(VI)-contaminated sites. Water Air Soil Pollut 226:180. https://doi.org/10.1007/s11270-015-2437-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Glasauer S, Langley S, Beveridge TJ (2002) Intracellular iron minerals in a dissimilatory iron-reducing bacterium. Science 295:117–119

    Article  CAS  PubMed  Google Scholar 

  • Gorby YA et al (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. In: Proceedings of the National Academy of Sciences, USA 103-11358-11363

  • Gotic M, Music S (2007) Mössbauer, FT-IT and Fe SEM investigation of iron oxides precipitated from FeSO4 solutions. J Mol Struct 834–836:445–453

    Article  Google Scholar 

  • Greenberger R, Mustard F, Cloutis E, Pratt L, Sauer P, Mann P, Turner K, Dyar D, Bish D (2015) Serpentinization, iron oxidation, and aqueous conditions in an ophiolite: implications for hydrogen production and habitability on Mars. Earth Planet Sci Lett 416:21–34

    Article  CAS  Google Scholar 

  • Grossman TH, Tuckman M, Ellestad S, Osburne MS (1993) Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfpo and Escherichia coli entD genes. J Bacteriol 175:6203–6211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansel CM, Benner SG, Neiss J, Dohnalkova A, Kukkadapu RK, Fendorf S (2003) Secondary mineralization pathways induced by dissimilatory iron reduction of ferrihydrite under advective flow. Geochim Cosmochim Acta 67:2977–2992

    Article  CAS  Google Scholar 

  • Hashimoto H, Yokoyama S, Asaoka H, Kusano Y, Ikeda Y, Seno M, Takada J, Fujii T, Murakami R (2007) Characteristics of hollow microtubes consisting of amorphous iron oxide nanoparticles produced by iron oxidizing bacteria, Leptothrix ochracea. J Magn Magn Mater 310:2405–2407

    Article  CAS  Google Scholar 

  • Hem JD, Cropper WH (1959) Survey of ferrous-ferric chemical equilibria and redox potentials. In: Chemistry of iron in natural water, geological survey water-supply paper 1459, The United States geological survey, 1962

  • Hong H, Kim SJ, Min UG, Lee YJ, Kim SG, Jung MY, Seo YS, Rhee SK (2015) Geosporobacter ferrireducens sp. nov., an anaerobic iron-reducing bacterium isolated from an oil-contaminated site. Antonie Van Leeuwenhoek 107:971–977

    Article  CAS  PubMed  Google Scholar 

  • Hosgormez H, Etiope G, Yalçin MN (2008) New evidence for a mixed inorganic and organic origin of the Olympic Chimaera fire (Turkey): a large onshore seepage of abiotic gas. Geofluids 8:263–273

    Article  CAS  Google Scholar 

  • Ionescu D, Heim C, Polerecky L, Thiel V, De Beer D (2015) Biotic and abiotic oxidation and reduction of iron at circumneutral pH are inseparable processes under natural conditions. Geomicrobiol J 32:221–230

    Article  CAS  Google Scholar 

  • Itävaara M, Nyyssönen M, Kapanen A, Nousiainen A, Ahonen L, Kukkonen I (2011) Characterization of bacterial diversity to a depth of 1500 m in the Outokumpu deep borehole, Fennoscandian Shield. FEMS Microbiol Ecol 77:295–309

    Article  PubMed  Google Scholar 

  • Kallmeyer J, Pockalny R, Adhikari R, Smith D, D’Hondt S (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. PNAS 40:16213–16216

    Article  Google Scholar 

  • Katsen-Globa A, Puetz N, Gepp MM, Neubauer JC, Zimmermann H (2016) Study of SEM preparation artefacts with correlative microscopy: cell shrinkage of adherent cells by HMDS-drying. Scanning 38:625–633

    Article  CAS  PubMed  Google Scholar 

  • Konhauser KO (1998) Diversity of bacterial iron mineralization. Earth-Sci Rev 43:91–121

    Article  CAS  Google Scholar 

  • Kotelnikova S (2002) Microbial production and oxidation of methane in the deep subsurface. Earth Sci Rev 58:367–395

    Article  CAS  Google Scholar 

  • Kwon MJ, O’Loughlin EJ, Boyanov MI, Brulc JM, Johnson ER, Kemner KM, Antonopoulos DA (2016) Impact of organic carbon electron donors on microbial community development under iron- and sulfate-reducing conditions. PLoS ONE 11:e0146689. https://doi.org/10.1371/journal.pone.0146689

    Article  PubMed  PubMed Central  Google Scholar 

  • Lentini CJ, Wankel SD, Hansel CM (2012) Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Front Microbiol 3:404

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Millero FJ (1999) The solubility of iron hydroxide in sodium chloride solutions. Geochim Cosmochim Acta 63:3487–3497

    Article  CAS  Google Scholar 

  • Lovley DR, Malvankar NS (2015) Seeing is believing: novel imaging techniques help clarify microbial nanowire structure and function. Environ Microbiol 17:2209–2215

    Article  CAS  PubMed  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matlakowska R, Skłodowska A, Nejbert K (2012) Bioweathering of Kupferschiefer black shale (Fore-Sudetic Monocline, SW Poland) by indigenous bacteria: implication for dissolution and precipitation of minerals in deep underground mine. FEMS Microbiol Ecol 81:99–110

    Article  CAS  PubMed  Google Scholar 

  • McIntyre NS, Zetaruk DG (1977) X-ray photoelectron spectroscopic studies of iron oxides. Anal Chem 49:1521–1529

    Article  CAS  Google Scholar 

  • McMillan DGG, Velasquez I, Nunn BL, Goodlett DR, Hunter KA, Lamont I, Sander SG, Cook GM (2010) Acquisition of iron by alkaliphilic Bacillus species. Appl Environ Microbiol 76:6955–6961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrill PL, Gijs Kuenen J, Johnson OJ, Suzuki S, Rietze A, Sessions AL, Fogel ML, Nealson KH (2013) Geochemistry and geobiology of a present-day serpentinization site in California: The Cedars. Geochim Cosmochim Acta 109:222–240

    Article  CAS  Google Scholar 

  • Morrill PL, Brazelton WJ, Kohl L, Rietze A, Miles SM, Kavanagh H, Schrenk MO, Ziegler SE, Lang SQ (2014) Investigations of potential microbial methanogenic and carbon monoxide utilization pathways in ultra-basic reducing springs associated with present-day continental serpentinization: the Tablelands, NL, CAN. Front Microbiol 5:1–13

    Article  Google Scholar 

  • Moser DP, Gihring TM, Brockman FJ, Fredrickson JK, Balkwill DL, Dollhopf ME et al (2005) Desulfotomaculum and Methanobacterium spp. dominate a 4- to 5-kilometer-deep fault. Appl Environ Microbiol 71:8773–8783. https://doi.org/10.1128/AEM.71.12.8773-8783.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Namduri H, Nasrazadani S (2008) Quantitative analysis of iron oxides using Fourier transform infrared spectrophotometry. Corros Sci 50:2493–2497

    Article  CAS  Google Scholar 

  • Nation JL (1983) A new method using hexamethyldisilazane for preparation of soft insect tissues for scanning electron microscopy. Biotech Histochem 58:347–351

    CAS  Google Scholar 

  • Neal C, Stanger G (1983) Hydrogen generation from mantle source rocks in Oman. Earth Planet Sci Lett 66:315–320

    Article  CAS  Google Scholar 

  • Neal C, Stanger G (1984) Calcium and magnesium hydroxide precipitation from alkaline groundwaters in Oman, and their significance to the process of serpentinization. Mineral Mag 48:237–241

    Article  CAS  Google Scholar 

  • Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548–572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Sullivan LA, Roussel EG, Weightman AJ, Webster G, Hubert CRJ, Bell E, Head I, Sass H, Parkes RJ (2015) Survival of Desulfotomaculum spores from estuarine sediments after serial autoclaving and high-temperature exposure. ISME J 9:922–933

    Article  PubMed  Google Scholar 

  • Ogg CD, Pael BK (2009) Thermotalea metallivorans gen. nov., sp. nov., a thermophilic, anaerobic bacterium from the Great Artesian Basin of Australia aquifer. IJSEM 59:964–971

    CAS  PubMed  Google Scholar 

  • Perez-Rodriguez I, Rawls M, Coykendall DK, Foustoukos DI (2016) Deferrisoma palaeochoriense sp. nov., a thermophilic, iron(III)-reducing bacterium from a shallow-water hydrothermal vent in the Mediterranean Sea. IJSEM 66:830–836

    CAS  PubMed  Google Scholar 

  • Posth NR, Canfield DE, Kappler A (2014) Biogenic Fe(III) minerals: from formation to diagenesis and preservation in the rock record. Earth Sci Rev 135:103–121

    Article  CAS  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3):e9490

    Article  PubMed  PubMed Central  Google Scholar 

  • Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    Article  CAS  PubMed  Google Scholar 

  • Reguera G, Nevin KP, Nicoll JS, Covalla SF, Woodard TL, Lovley DR (2006) Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 72:7345–7348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roden EE (2012) Microbial iron-redox cycling in subsurface environments. Biochem Soc Trans 40:1249–1256

    Article  CAS  PubMed  Google Scholar 

  • Roden EE, Sobolev D, Glazer B, Luther GW (2004) Potential for microscale bacterial Fe redox cycling at the aerobic–anaerobic interface. Geomicrobiol J 21:379–391

    Article  CAS  Google Scholar 

  • Roden EE, McBeth JM, Blothe M, Percak-Dennett EM, Fleming EJ, Holyoke RR, Luther GWIII, Emerson D, Schieber J (2012) The microbial ferrous wheel in a neutral pH groundwater seep. Front Microbiol 3:172

    Article  PubMed  PubMed Central  Google Scholar 

  • Roh Y, Chon CM, Moon JW (2007) Metal reduction and biomineralization by an alkaliphilic metal-reducing bacterium, Alkaliphilus metalliredigens (QYMF). Geosci J 11:415–423

    Article  CAS  Google Scholar 

  • Rowe AR, Yoshimura M, LaRowe DE, Bird LJ, Amend JP, Hashimoto K, Nealson KH, Okamoto A (2017) In situ electrochemical enrichment and isolation of a magnetite-reducing bacterium from a high pH serpentinizing spring. Environ Microbiol 19:2272–2285

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Murillo R, Gazel E, Schwarzenbach EM, Crespo-Medina M, Schrenk MO, Boll J, Gill BC (2014) Geochemical evidence for active tropical serpentinization in the Santa Elena ophiolite, Costa Rica: an analog of a humid early Earth? Geochem Geophys Geosyst 15:1783–1800. https://doi.org/10.1002/2013GC005213

    Article  CAS  Google Scholar 

  • Sawicki J, Brown D, Beveridge T (1995) Microbial precipitation of siderite and protoferrihydrite in a biofilm. Can Mineral 33:1–6

    CAS  Google Scholar 

  • Schädler S, Burkhardt C, Hegler F, Straub KL, Miot J, Benzerara K, Kappler A (2009) Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria. Geomicrobiol J 26:93–103

    Article  Google Scholar 

  • Schrenk MO, Kelly DS, Delaney JR, Baross JA (2003) Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl Environ Microbiol 69:3580–3592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schrenk MO, Brazelton W, Lang S (2013) Serpentinization, carbon, and deep life. Rev Mineral Geochem 75:575–606

    Article  CAS  Google Scholar 

  • Shervais J, Choi SH (2011) Subduction initiation along transform faults: the proto-Franciscan subduction zone. Lithosphere 4:484–496

    Article  Google Scholar 

  • Stevens TO, McKinley JP (1995) Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270:450

    Article  CAS  Google Scholar 

  • Suzuki S, Ishii S, Wu A, Cheung A, Tenny A, Wagner G, Kuenen JG, Nealson KH (2013) Microbial diversity in The Cedars, an ultrabasic, ultrareducing, and low salinity serpentinizing ecosystem. Proc Natl Acad Sci 110:15336–15341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki S, Kuenen JG, Schipper K, van der Velde S, Ishii SI, Wu A, Sorokin AT, Meng X, Morill PL, Kamagata Y, Muyzer G, Nealson KH (2014) Physiological and genomic features of highly alkaliphilic hydrogen-utilizing Betaproteobacteria from a continental serpentinizing site. Nat Commun 5:1–12

    CAS  Google Scholar 

  • Swanner ED, Wu W, Hao L, Wustner ML, Obst M, Moran DM, McIIvin MR, Saito MA, Kappler A (2015) Physiology, Fe(II) oxidation, and Fe mineral formation by a marine planktonic cyanobacterium grown under ferruginous conditions. Front Earth Sci 3:60

    Article  Google Scholar 

  • Szponar N, Brazelton WJ, Schrenk MO, Bower DM, Steele A, Morrill PL (2013) Geochemistry of a continental site of serpentinization, the Tablelands ophiolite, Gros Morne National Park: a Mars analogue. Icarus 224:286–296

    Article  CAS  Google Scholar 

  • Tiago I, Veríssimo A (2013) Microbial and functional diversity of a subterrestrial high pH groundwater associated to serpentinization. Environ Microbiol 15:1687–1706

    Article  CAS  PubMed  Google Scholar 

  • Twing KI, Brazelton WJ, Kubo MDY, Hyer AJ, Cardace D, Hoeler TM, McCollom TM, Schrenk MO (2017) Serpentinization-influenced groundwater harbors extremely low diversity microbial communities adapted to high pH. Front Microbiol 8:308

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Hu C, Zhang L, Li X, Zhang Y, Yang M (2014) Effects of microbial redox cycling of iron on cast iron pipe corrosion in drinking water distribution systems. Water Res 65:362–370

    Article  CAS  PubMed  Google Scholar 

  • Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764

    Article  CAS  PubMed  Google Scholar 

  • Williams AJ, Sumner DY, Alpers CN, Karunatillake S, Hofmann BA (2015) Preserved filamentous microbial biosignatures in the Brick Flat gossan, Iron Mountain, CA. Astrobiology 15:637–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams AJ, Alpers CN, Sumner DY, Campbell K (2017) Filamentous hydrous ferric oxide biosignatures in a pipeline carrying acid mine drainage at iron Mountain Mine, California. Geomicrobiol J 34:193–206. https://doi.org/10.1080/01490451.2016.1155679

    Article  CAS  Google Scholar 

  • Williamson AJ, Morris K, Shaw S, Byrne JM, Boothman C, Lloyd JR (2013) Microbial reduction of Fe(III) under alkaline conditions relevant to geological disposal. Appl Environ Microbiol 79:3320–3326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woycheese KM, Meyer-Dombard DM, Cardace D, Arcilla C (2015) Out of the dark: transitional subsurface-to-surface microbial diversity in a terrestrial serpentinizing seep (Manleluag, Pangasinan, the Philippines). Front Microbiol 6:1–12

    Article  Google Scholar 

  • Ye Q, Roh Y, Carroll SL, Blair B, Zhou J, Zhang CL, Fields MW (2004) Alkaline anaerobic respiration: isolation and characterization of a novel alkaliphilic and metal-reducing bacterium. Appl Environ Microbiol 70:5595–5602

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work would not have been possible without the generous support of NSF Grant #s 1147334 and 1146910 to DRMD and DC, respectively. Further funding was awarded to DRMD by the Illinois Space Grant Consortium in support of student research. Student travel funding was awarded to CPC (Knourek Scholarship). The authors would like to acknowledge Gamaliel Lysander Benig Cabria, Bharathi Vallalar, Kristin Woycheese, Karmina Aquino, Jeffrey Munar, and Emmanuel Codillo for their tireless efforts in the field. The authors would like to further thank Drs. S. Guggenheim and F. Kenig for guidance, and Dr. S. Green, Olivia Thompson, Tad Daniel, and Ankur Naqib for technical and analytical support. This is EDGElab contribution #4.

Author information

Authors and Affiliations

  1. Department of Earth and Environmental Sciences, University of Illinois at Chicago, m/c 186, 845 W. Taylor St., Chicago, IL, 60515, USA

    D’Arcy R. Meyer-Dombard, Caitlin P. Casar & Alexander G. Simon

  2. Department of Geosciences, University of Rhode Island, Kingston, IL, USA

    Dawn Cardace

  3. Department of Earth and Environmental Sciences, Michigan State University, East Lansing, MI, USA

    Matthew O. Schrenk

  4. Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, USA

    Matthew O. Schrenk

  5. National Institute of Geological Sciences, University of the Philippines, Diliman, Quezon City, Philippines

    Carlo A. Arcilla

Authors
  1. D’Arcy R. Meyer-Dombard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caitlin P. Casar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander G. Simon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dawn Cardace
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matthew O. Schrenk
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carlo A. Arcilla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D’Arcy R. Meyer-Dombard.

Additional information

Communicated by F. Robb.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 15198 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meyer-Dombard, D.R., Casar, C.P., Simon, A.G. et al. Biofilm formation and potential for iron cycling in serpentinization-influenced groundwater of the Zambales and Coast Range ophiolites. Extremophiles 22, 407–431 (2018). https://doi.org/10.1007/s00792-018-1005-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-018-1005-z

Keywords

Search

Navigation