Isolation and Characterization of Novel Iron-Oxidizing Autotrophic and Mixotrophic Bacteria from Boiling Springs Lake, an Oligotrophic, Acidic Geothermal Habitat

References

• Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402.
   PubMed Web of Science ®Google Scholar
• Atlas RM. 2004. Handbook of Microbiological Media. Boca Raton, FL: CRC Press.
   Google Scholar
• Bai Y, Wang J, Zhang Z, Shi P, Luo H, Huang H, Feng Y, Yao B. 2010a. Extremely acidic β-1,4-glucanase, CelA4, from thermoacidophilic Alicyclobacillus sp. A4 with high protease resistance and potential as a pig feed additive. J Agric Food Chem 58:1970–1975.
   PubMed Web of Science ®Google Scholar
• Bai Y, Wang J, Zhang Z, Shi P, Luo H, Huang H, Luo C, Yao B. 2010b. A novel family 9 β-1,3(4)-glucanase from thermoacidophilic Alicyclobacillus sp. A4 with potential applications in the brewing industry. Appl Microbiol Biotech 87:251–259.
   PubMed Web of Science ®Google Scholar
• Bai Y, Wang J, Zhang Z, Yang P, Shi P, Luo H, Meng K, Huang H, Yao B. 2010c. A new xylanase from thermoacidophilic Alicyclobacillus sp. A4 with broad-range pH activity and pH stability. J Ind Microbiol Biotech 37:187–194.
   PubMed Web of Science ®Google Scholar
• Baker BJ, Banfield JF. 2003. Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152.
   PubMed Web of Science ®Google Scholar
• Balkwill DL, Ghiorse WC. 1985. Characterization of subsurface bacteria associated with two shallow aquifers in Oklahoma. Appl Environ Microbiol 50:580–588.
   PubMed Web of Science ®Google Scholar
• Bogdanova TI, Tsaplina IA, Kondrat’eva TF, Duda VI, Suzina NE, Melamud VS, Tourova TP and Karavaiko, GI. 2006. Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium. Int J Syst Evol Microbiol 56:1039–1042.
   PubMed Web of Science ®Google Scholar
• Boyd, ES, Leavitt, WD, Geesey, GG. 2009. CO2 uptake and fixation by a thermoacidophilic microbial community attached to precipitated sulfur in a geothermal spring. Appl. Environ Microbiol 75:4289–4296.
   Web of Science ®Google Scholar
• Bridge TAM, Johnson DB. 1998. Reduction of soluble iron and reductive dissolution of ferric iron-containing minerals by moderately thermophilic iron-oxidizing bacteria. Appl. Environ Microbiol 64:2181–2186.
   Web of Science ®Google Scholar
• Brierley JA. 1978. Thermophilic iron-oxidizing bacteria found in copper leaching dumps. Appl. Environ Microbiol 36:523–525.
   Web of Science ®Google Scholar
• Clark DA, Norris PR. 1996. Acidimicrobium ferrooxidans gen. nov., sp. nov. : mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785–790.
   PubMed Web of Science ®Google Scholar
• Cleaver AA, Burton NP, Norris PR. 2007. A novel Acidimicrobium species in continuous cultures of moderately thermophilic, mineral-sulfide-oxidizing acidophiles. Appl Environ Microbiol 73:4294–4299.
   PubMed Web of Science ®Google Scholar
• Di Lauro B, Rossi M, Moracci M. 2006. Characterization of a β-glycosidase from the thermoacidophilic bacterium Alicyclobacillus acidocaldarius. Extremophiles 10:301–310.
   PubMed Web of Science ®Google Scholar
• Druschel GK, Baker BJ, Gihring TM, Banfield JF. 2004. Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem Trans 5:13–32.
   PubMed Web of Science ®Google Scholar
• Ehrlich HL, Newman DK. 2009. Geomicrobiology. Boca Raton, FL, CRC Press.
   Google Scholar
• Evangelou, VP. 1995. Pyrite Oxidation and its Control. New York: CRC Press.
   Google Scholar
• Falagán C, Sánchez-España J, Johnson DB. 2014. New insights into the biogeochemistry of extremely acidic environments revealed by a combined cultivation-based and culture-independent study of two stratified pit lakes. FEMS Microbiol Ecol 87:231–243.
   PubMed Web of Science ®Google Scholar
• Golovacheva RS, Karavaiko GI. 1978. Sulfobacillus, a new genus of thermophilic sporeforming bacteria. Mikrobiologiia [in Russian] 47:815–822.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amiles R. 2003. Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69:4853–4865.
   PubMed Web of Science ®Google Scholar
• Hansen MC, Toker-Neilson T, Givskov M, Molin S. 1998. Biased 16S rDNA PCR amplification caused by interference from DNA flanking template region. FEMS Microbiol Ecol 26:141–149.
   Web of Science ®Google Scholar
• Hedrich S, Johnson DB. 2013. Aerobic and anaerobic oxidation of hydrogen by acidophilic bacteria. FEMS Microbiol Lett 349:40–45.
   PubMed Web of Science ®Google Scholar
• Hudson CL. 2012. Determination of antibiotic resistance in the bacterial community of Boiling Springs Lake in Lassen Volcanic National Park. M. S. thesis, Humboldt State University, Arcata, California.
   Google Scholar
• Johnson DB. 1995. Selective solid media for isolating and enumerating acidophilic bacteria. J Micro Methods 23:205–218.
   Web of Science ®Google Scholar
• Johnson DB. 2008. Carbon, iron and sulfur metabolism in acidophilic micro-organisms. Advan Microb Phys 54:201–255.
   Web of Science ®Google Scholar
• Johnson DB. 2012. Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 81:2–12.
   PubMed Web of Science ®Google Scholar
• Johnson DB, Joulian C, d’Hugues P, Hallberg KB. 2008. Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations. Extremophiles 12: 789–798.
   PubMed Web of Science ®Google Scholar
• Johnson DB, Kanao T, Hedrich S. 2012. Redox transformations of iron at extremely low pH: fundamental and applied aspects. Front Microbiol 3:96.
   PubMed Web of Science ®Google Scholar
• Johnson DB Okibe N, Roberto FF. 2003. Novel thermo-acidophilic bacteria isolated from geothermal sites in Yellowstone National Park: physiological and phylogenetic characteristics. Arch Microbiol 180:60–68.
   PubMed Web of Science ®Google Scholar
• Karavaiko GI, Bogdanova TI, Tourova TP, Kondrat’eva TF, Tsaplina IA, Egorova MA, Krasil’nikova EN, Zakharchuk LM. 2005. Reclassification of Sulfobacillus thermosulfidooxidans subsp. thermotolerans strain K1 as Alicyclobacillus tolerans sp. nov. and Sulfobacillus disulfidooxidans Dufresne et al. 1996 as Alicyclobacillus disulfidooxidans comb. nov., and emended description of the genus Alicyclobacillus. Int. J Syst Evol Microbiol 55: 941–947.
   PubMed Web of Science ®Google Scholar
• Lane DJ. 1991. 16S/23S rRNA sequencing. In Stackerbrandt E, Goodfellow M, editors. Nucleic Acid Techniques in Bacterial Systematics. Chichester, UK, Wiley, p115–175.
   Google Scholar
• Lees H, Kwok SC, Suxuki I. 1969. The thermodynamics of iron oxidation by the ferrobacilli. Can J Microbiol 15:43–46.
   PubMed Web of Science ®Google Scholar
• Lovley DR, Phillips EJP. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540.
   PubMed Web of Science ®Google Scholar
• Macalady JL, Jones DS, Lyon EH. 2007. Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ Microbiol 9:1402–1414.
   PubMed Web of Science ®Google Scholar
• Melamud VS, Pivovarova TA, Tourova TP, Kolganova TV, Osipov GA, Lysenko AM, Kondrat’eva TF, Karavaiko GI. 2003. Sulfobacillus sibiricus sp. nov., a new moderately thermophilic bacterium. Microbiology 72:605–612.
   Web of Science ®Google Scholar
• Morana A, Esposito A, Maurelli L, Ruggiero G, Ionata E, Rossi M, La Cara F. 2008. A novel thermoacidophilic cellulase from Alicyclobacillus acidocaldarius. Prot Pep Lett 15:1017–1021.
   PubMed Web of Science ®Google Scholar
• Murr L. 2006. Biological issues in materials science and engineering: interdisciplinarity and the bio-materials paradigm. JOM 58:23–33.
   Web of Science ®Google Scholar
• Norris PR, Barr DW. 1985. Growth and iron oxidation by acidophilic moderate thermophiles. FEMS Microbiol Lett 28:221–224.
   Web of Science ®Google Scholar
• Norris PR, Clark DA, Owen JP, Waterhouse S. 1996. Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology 142:775–783.
   PubMed Web of Science ®Google Scholar
• Okibe N, Gericke M, Hallberg KB, Johnson DB. 2003. Enumeration and characterization of acidophilic microorganisms isolated from a pilot plant stirred-tank bioleaching operation. Appl Environ Microbiol 69:1936–1943.
   PubMed Web of Science ®Google Scholar
• Reynolds ES. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol 17: 208–212.
   PubMed Web of Science ®Google Scholar
• Reysenbach A-L, Pace NR. 1995. Reliable amplification of hyperthermophilic Archaeal 16S rRNA genes by the polymerase chain reaction. In: Robb FT, Place AR, editors. Archaea- A Laboratory Manual (Thermophiles).Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press, p101–106.
   Google Scholar
• Rheims H, Spröer C, Rainey FA, Stackebrandt E. 1996. Molecular biological evidence for the occurrence of uncultured members of the actinomycete line of descent in different environments and geographical locations. Microbiology 142:2863–2870.
   PubMed Web of Science ®Google Scholar
• Sand W, Gerke, T, Hallmann R, Schippers A. 1995. Sulfur chemistry, biofilm, and the (in) direct attack mechanism; a critical evaluation of bacterial leaching. Appl Microbiol Biotechnol 43:961–966.
   Web of Science ®Google Scholar
• Santofimia E, Gonzalez-Toril E, Lopez-Pamo E, Gomariz M, Amils R, Aguiler, A. 2013. Microbial diversity and its relationship to physicochemical characteristics of the water in two extreme acidic pit lakes from the Iberian Pyrite Belt (SW Spain). PLoS One 8: e66746.
   PubMed Web of Science ®Google Scholar
• Shade A, Hogan CS, Klimowicz AK, Linske M, McManus PS, Handelsman J. 2012. Culturing captures members of the soil rare biosphere. Environ Microbiol 14:2247–2252.
   PubMed Web of Science ®Google Scholar
• Siering PL, Clarke JM, Wilson MS. 2006. Geochemical and biological diversity of acidic, hot springs in Lassen Volcanic National Park. Geomicrobiol J 23:129–141.
   Web of Science ®Google Scholar
• Siering PL, Wolfe GV, Wilson MS, Yip AN, Carey CM, Wardman CD, Shapiro RS, Stedman KM, Kyle JE, Yuan T, Van Nostrand JD, He Z, Zhou J. 2013. Microbial biogeochemistry of Boiling Springs Lake: a physically dynamic, oligotrophic, low pH geothermal ecosystem. Geobiology 11:356–376.
   PubMed Web of Science ®Google Scholar
• Silverman MP, Lundgren DG. 1959. Studies on the chemoautorophic iron bacterium Ferrobacillus ferrooxidans II. J Bacteriol 78:326–331.
   PubMed Web of Science ®Google Scholar
• Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680.
   PubMed Web of Science ®Google Scholar
• Wang J, Bai Y, Shi P, Luo H, Huang H, Yin J, Yao B. 2011. A novel xylanase, XynA4-2, from thermoacidophilic Alicyclobacillus sp. A4 with potential applications in the brewing industry. World J Microbiol Biotech 27:207–213.
   Web of Science ®Google Scholar
• Wilson MS, Siering PL, White CL, Hauser ME, Bartles AN. 2008. Novel Archaea and Bacteria dominate stable microbial communities in North America's largest hot spring Microb Ecol 56:292–305.
   PubMed Web of Science ®Google Scholar
• Wood AP, Kelly DP. 1983. Autotrophic and mixotrophic growth of three thermoacidophilic iron-oxidizing bacteria. FEMS Microbiol Lett 20:107–112.
   Web of Science ®Google Scholar
• Wolfe GW, Fitzhugh C, Almasary A, Green A, Bennett P, Wilson MS, Siering PL. 2014. Microbial heterotrophic production in an oligotrophic acidic geothermal lake: responses to organic amendments and terrestrial plant litter. FEMS Microb Ecol FEMSEC-14-03-0176.R1. In Press.
   Google Scholar
• Yacob T, Pandey S, Silverstein, J, Rajaram H. 2013. Soluble microbial products decrease pyrite oxidation by ferric iron at pH < 2. Environ Sci Technol 47:8658–8665.
   PubMed Web of Science ®Google Scholar