Does aspartic acid racemization constrain the depth limit of the subsurface biosphere?

Geobiology

Volumn 12, Issue 1, 2014, Pages 1-19

  Onstott, T C ^a,b   Magnabosco, C ^a,b   Aubrey, A D ^c   Burton, A S ^d   Dworkin, J P ^e   Elsila, J E ^e   Grunsfeld, S ^f   Cao, B H ^g   Hein, J E ^g   Glavin, D P ^e   Kieft, T L ^h   Silver, B J ⁱ   Phelps, T J ^j   van Heerden, E ^k   Opperman, D J ^k   Bada, J L ^l  

^a PRINCETON UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d NASA JOHNSON SPACE CENTER   (United States)

^e NASA GODDARD SPACE FLIGHT CENTER   (United States)

^f River Hill High School   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h NEW MEXICO INSTITUTE OF MINING AND TECHNOLOGY   (United States)

ⁱ ARCADIS   (United States)

^j OAK RIDGE NATIONAL LABORATORY   (United States)

^k UNIVERSITY OF THE FREE STATE   (South Africa)

^l UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; AMINO ACID; ASPARTIC ACID; BIOSPHERE; MAINTENANCE; PROTEIN; RACEMIZATION; SURVIVAL; TURNOVER;

SOUTH AFRICA;

BACTERIA (MICROORGANISMS);

ASPARTIC ACID; BACTERIAL DNA;

ARTICLE; BACTERIUM; CELL DIVISION; CHEMISTRY; CYTOLOGY; DNA SEQUENCE; GENETICS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEDIMENT; SOUTH AFRICA; TEMPERATURE; TIME;

ASPARTIC ACID; BACTERIA; CELL DIVISION; DNA, BACTERIAL; GEOLOGIC SEDIMENTS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SOUTH AFRICA; TEMPERATURE; TIME FACTORS;

EID: 84890222423     PISSN: 14724677     EISSN: 14724669     Source Type: Journal    
DOI: 10.1111/gbi.12069     Document Type: Article

References (91)

1. Arbige M, Chesbro W (1982) relA and related loci are growth rate determinants for Escherichia coli in a recycling fermenter. Journal of General Microbiology 128, 693-703.
2. Atlas RM (1993) Handbook of Microbiological Media. CRC Press, Boca Raton, FL.
3. Aubrey AD (2008) Amino acid biosignatures: implications for the detection of extinct or extant microbial communities on Mars. Ph.D. Thesis, Department of Oceanography. University of California, San Diego, p. 228.
4. Bada JL (1972) Kinetics of racemization of amino acids as a function of pH. Journal of the American Chemical Society 94, 1371-1373.
5. Bada JL (1982) Racemization of amino acids in nature. Interdisciplinary Science Reviews 7, 30-46.
6. Bada JL (1984) In vivo racemization in mammalian proteins. Methods in Enzymology 106, 98-115.
7. Bada JL, Schroeder RA (1975) Amino acid racemization reactions and their geochemical implications. Naturwissenschaften 62, 71-79.
8. Bada JL, Wang XYS, Hamilton H (1999) Preservation of key biomolecules in the fossil record: current knowledge and future challenges. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 354, 77-86.
9. Boone DR, Liu Y, Zhao Z-J, Balkwill DL, Drake GR, Stevens TO, Aldrich HC (1995) Bacillus infernus sp. nov., an Fe(II1)- and Mn(1V)-Reducing Anaerobe from the Deep Terrestrial Subsurface. International Journal of Systematic Bacteriology 45, 441-448.
10. Borgonie G, García-Moyano A, Litthauer D, Bert W, Bester A, Heerden Ev, Onstott TC (2011) Nematoda from the terrestrial deep subsurface of South Africa. Nature 474, 79-82.
11. Brinton KLF, Tsapin AI, Gilichinsky D, McDonald GD (2002) Aspartic acid racemization and age-depth relationships for organic carbon in Siberian permafrost. Astrobiology 2, 77-82.
12. Butlin KR, Adams ME, Thomas M (1949) The isolation and cultivation of sulfate-reducing bacteria. Microbiology 3, 46-59.
13. Chivian D, Alm E, Brodie E, Culley D, Dehal P, DeSantis T, Gihring T, Lapidus A, Lin L-H, Lowry S, Moser D, Richardson P, Southam G, Wanger G, Pratt L, Andersen G, Hazen T, Brockman F, Arkin A, Onstott T (2008) Environmental genomics reveals a single species ecosystem deep within the Earth. Science 322, 275-278.
14. Colwell FS, D'Hondt S (2013) Nature and Extent of the Deep Biosphere. In Carbon in Earth. (eds Hazen RM, Jones AP, Baross JA). Mineralogical Society of America, Chantilly, VA, pp. 547-566.
15. Colwell FS, Boyd S, Delwiche ME, Reed DW, Phelps TJ, Newby DT (2008) Estimates of biogenic methane production rates in deep marine sediments at hydrate ridge, cascadia margin. Applied and Environment Microbiology 74, 3444-3452.
16. Connan J (1984) Biodegradation of crude oils in reservoirs. In Advances in Petroleum Geochemistry. (eds Brooks J, Welte DH). Academic Press, London, pp. 299-330.
17. Davidson MM, Bisher ME, Pratt LM, Fong J, Southam G, Pfiffner SM, Reches Z, Onstott TC (2009) Sulfur isotope enrichment during maintenance metabolism in the thermophilic sulfate-reducing bacterium Desulfotomaculum putei. Applied and Environment Microbiology 75, 5621-5630.
18. D'Hondt S, Rutherford S, Spivack AJ (2002) Metabolic activity of subsurface life in deep-sea sediments. Science 295, 2067-2070.
19. Dill KA, Ghosh K, Schmit JD (2011) Physical limits of cells and proteomes. Proceedings of the National Academy of Sciences of the USA 108, 17876-17882.
20. Fishbain S, Dillon J, Gough HL, Stahl DA (2003) Linkage of high rates of sulfate reduction in Yellowstone hot springs to unique sequence types in the dissimilatory sulfate respiration pathway. Applied and Environmental Microbiology 69, 3663-3667.
21. Geiger T, Clarke S (1987) Deamidation, isomerization, and racemization at Asparaginyl and Aspartyl residues in peptides. The Journal of Biological Chemistry 262, 785-794.
22. Gihring TM, Moser DP, Lin L-H, Davidson MM, Onstott TC, Morgan L, Milleson M, Kieft T, Trimarco E, Balkwill DL, Dollhopf M (2006) The distribution of microbial taxa in the subsurface water of the Kalahari Shield, South Africa. Geomicrobiology Journal 23, 415-430.
23. Glavin DP, Schubert M, Botta O, Kminek G, Bada JL (2001) Detecting pyrolysis products from bacteria on Mars. Earth and Planetary Science Letters 185, 1-5.
24. Glavin DP, Dworkin JP, Aubrey A, Botta O, Doty JH III, Martins Z, Bada JL (2006) Amino acid analyses of Antarctic CM2 meteorites using liquid chromatography-time of flight-mass spectrometry. Meteoritics & Planetary Science 41, 889-902.
25. Glavin DP, Aubrey AD, Callahan MP, Dworkin JP, Elsila JE, Parker ET, Bada JL, Jennisken P, Shaddad MH (2010) Extraterrestrial amino acids in the Almahata Sitta meteorite. Meteoritics & Planetary Science 45, 1695-1709.
26. Greaves RB, Warwicker J (2007) Mechanisms for stabilisation and the maintenance of solubility in proteins from thermophiles. BMC Structural Biology 7, 18.
27. Grutters M, van Raaphorst W, Epping E, Helder W, de Leeuw JW, Glavin DP, Bada J (2002) Preservation of amino acids from in situ-produced bacterial cell wall peptidoglycans in northeastern Atlantic continental margin sediments. Limnology and Oceanography 47, 1521-1524.
28. Haas BJ, Sandigursky M, Tainer JA, Franklin WA, Cunningham RP (1999) Purification and characterization of Thermotoga maritima endonuclease IV, a thermostable apurinic/apyrimidinic endonuclease and 39-repair diesterase. Journal of Bacteriology 181, 2834-2839.
29. Habicht KS, Canfield DE (1996) Sulphur isotope fractionation in modern microbial mats and the evolution of the sulphur cycle. Nature 382, 342-343.
30. Habicht KS, Salling L, Thamdrup B, Canfield DE (2005) Effect of low sulfate concentrations on lactate oxidation and isotope fractionation during sulfate reduction by archaeoglobus fulgidus strain Z†. Applied and Environment Microbiology 71, 3770-3777.
31. Hayashi R, Kameda I (1980) Racemization of amino acid residues during alkali-treatment of protein and its adverse effect on pepsin digestibility. Agricultural Biological Chemistry 44, 891-895.
32. Heijnen JJ, van Dieken JP (1992) In search of a thermodynamic description of biomass yields for the chemotrophic growth of microorganisms. Biotechnology and Bioengineering 39, 833-858.
33. Hoehler TM (2004) Biological energy requirements as quantitative boundary conditions for life in the subsurface. Geobiology 2, 205-215.
34. Jin Q, Bethke CM (2005) Predicting the rate of microbial respiration in geochemical environments. Geochimica et Cosmochimica Acta 69, 1133-1143.
35. Kaboev OK, Luchkina LA, Kuziakin TI (1985) Apurinic and apyrimidinic DNA endonuclease of extremely thermophilic Thermothrix thiopara. Journal of Bacteriology 164, 878-881.
36. Kaiser K, Benner R (2005) Hydrolysis-induced racemization of amino acids. Limnology and Oceanography: Methods 3, 318-325.
37. Kallmeyer J, Smith D, D'Hondt S, Spivack A (2008) New cell extraction procedure applied to deep subsurface sediments. Limnology and Oceanography: Methods 6, 236-245.
38. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D'Hondt S (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. Proceedings of the National Academy of Sciences of the USA 109, 16213-16216.
39. Kandler O, Konig H (1978) Chemical composition of the peptidoglycan-free cell walls of methanogenic bacteria. Archives of Microbiology 118, 141-152.
40. Kieft T, McCuddy S, Onstott T, Davidson M, Lin L-H, Mislowack B, Pratt L, Boice E, Sherwood Lollar B, Lippmann-Pipke J, Pfiffner S, Phelps T, Gihring T, Moser D, van Heerden A (2005) Geochemically generated, energy-rich substrates and indigenous microorganisms in deep, ancient groundwater. Geomicrobiology Journal 22, 325-355.
41. Kjelleberg S, Hermansson M, Mårdén P, Jones GW (1987) The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment. Annual Review of Microbiology 41, 25-49.
42. Larter S, Wilhelms A, Head I, Koopmans M, Aplin A, Primio RD, Zwach C, Erdmann M, Telnaes N (2003) The controls on the composition of biodegraded oils in the deep subsurface-part 1: biodegradation rates in petroleum reservoirs. Organic Geochemistry 34, 601-613.
43. L'Haridon S, Reysenbach A-L, Glenat P, Prieur D, Jeanton C (1995) Hot subterranean biosphere in a continental oil reservoir. Nature 377, 223-224.
44. Li J, Brill TB (2003) Spectroscopy of hydrothermal reactions part 26: kinetics of decarboxylation of aliphatic amino acids and comparison with the rates of racemization. International Journal of Chemical Kinetics 35, 602-610.
45. 2 in continental crust: nuclear power for deep subsurface microbial communities. Geochemistry Geophysics Geosystems 6, 1-13.
46. Lin LH, Wang P-L, Rumble D, Lippmann-Pipke J, Boice E, Pratt LM, Sherwood Lollar B, Brodie E, Hazen T, Andersen G, DeSantis T, Moser DP, Kershaw D, Onstott TC (2006) Long term biosustainability in a high energy, low diversity crustal biome. Science 314, 479-482.
47. Lindahl T, Nyberg B (1972) Rate of depurination of native deoxyribonucleic acid. Biochemistry 11, 3610-3618.
48. 36Cl, Witwatersrand Basin, South Africa. Geochimica et Cosmochimica Acta 67, 4597-4619.
49. Lippmann-Pipke J, Erzinger J, Zimmer M, Kujawa C, Boettcher M, Heerden EV, Bester A, Moller H, Stroncik NA, Reches Z (2011a) Geogas transport in fractured hard rock - Correlations with mining seismicity at 3.54 km depth, TauTona gold mine, South Africa. Applied Geochemistry 26, 2134-2146.
50. Lippmann-Pipke J, Sherwood Lollar B, Neidermann S, Stroncik N, Naumann R, VanHeerden E, Onstott TC (2011b) Neon identifies two billion year old fluid component in Kaapvaal Craton. Chemical Geology 282, 287-296.
51. Lomstein BA, Langerhuus AT, D'Hondt S, Jørgensen BB, Spivack AJ (2012) Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484, 101-104.
52. Masters PM, Bada JL, Zigler JS (1977) Aspartic acid racemisation in the human lens during ageing and in cataract formation. Nature 268, 71-73.
53. Matsumoto M, Homma H, Long Z, Imai K, Iida T, Maruyama T, Aikwa Y, Endo I, Yohda M (1999) Occurrence of free D-amino acids and aspartate racemases in hyperthermophilic archaea. Journal of Bacteriology 181, 6560-6563.
54. McCollom TM, Amend JP (2005) A thermodynamic assessment of energy requirements for biomass synthesis by chemolithoautotrophic micro-organisms in oxic and anoxic environments. Geobiology 3, 135-144.
55. Miroshnichenko ML, Hippe H, Stackebrandt E, Kostrikina NA, Chernyh NA, Jeanthon C, Nazina TN, Belyaev SS, Bonch-Osmolovskaya EA (2001) Isolation and characterization of Thermococcus sibiricus sp. nov. from a Western Siberia high-temperature oil reservoir. Extremophiles 5, 85-91.
56. Morita R (1997) Bacteria in Oligotrophic Environments: Starvation-Survival Lifestyle. Chapman and Hall, New York.
57. Moser DP, Gihring T, Fredrickson JK, Brockman FJ, Balkwill D, Dollhopf ME, Sherwood-Lollar B, Pratt LM, Boice E, Southam G, Wanger G, Welty AT, Baker BJ, Onstott TC (2005) Desulfotomaculum spp. and Methanobacterium spp. Dominate 4-5 km deep fault. Applied and Environmental Microbiology 71, 8773-8783.
58. Ohta E (1991) Polymetallic mineralization at the Toyoha mine, Hokkaido, Japan. Mining Geology 41, 279-295.
59. Onstott TC, Lin L-H, Davidson M, Mislowack B, Borcsik M, Hall J, Slater GF, Ward J, Sherwood Lollar B, Lippmann-Pipke J, Boice E, Pratt LM, Pfiffner SM, Moser DP, Gihring T, Kieft TL, Phelps TJ, van Heerden E, Litthaur D, DeFlaun M, Rothmel R (2006) The origin and age of biogeochemical trends in deep fracture water of the Witwatersrand Basin, South Africa. Geomicrobiology Journal 23, 369-414.
60. Onstott TC, van Heerden E, Murdoch L (2010) Microbial life in the depths of the earth. Géosciences, la revue du BRGM pour une Terre Durable 11, 52-59.
61. Parkes RJ, Cragg BA, Getliff JM, Harvey SM, Fry JC, Lewis CA, Rowland SJ (1993) A quantitative study of microbial decomposition of biopolymers in recent sediments from the Peru Margin. Marine Geology 113, 55-66.
62. Peters V, Janssen PH, Conrad R (1998) Efficiency of hydrogen utilization during unitrophic and mixotrophic growth of Acetobacterium woodii on hydrogen and lactate in the chemostat. FEMS Microbiology Ecology 26, 317-324.
63. Pfiffner SM, Cantu JM, Smithgall A, Peacock AD, White DC, Moser DP, Onstott TC, van Heerden E (2006) Deep subsurface microbial biomass and community structure in Witwatersrand Basin mines. Geomicrobiology Journal 23, 431-442.
64. Phelps TJ, Murphy EM, Pfiffner SM, White DC (1994) Comparison between geochemical and biological estimates of subsurface microbial activities. Microbial Ecology 28, 335-349.
65. Poinar HN, Höss M, Bada JL, Pääbo S (1996) Amino acid racemization and the preservation of ancient DNA. Science 272, 864-866.
66. Price PB, Sowers T (2004) Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proceedings of the National Academy of Science of the USA 101, 4631-4646.
67. Ram R, VerBerkmoes N, Thelen M, Tyson G, Baker B, Blake R, Manesh SM, Hettich R, Banfield J (2005) Community proteomics identifies key activities in a natural microbial biofilm. Science 308, 1915-1920.
68. Röling WFM, Head IM, Larter SR (2003) The microbiology of hydrocarbon degradation in subsurface petroleum reservoirs: perspectives and prospects. Research in Microbiology 154, 321-328.
69. Rosa C, Zeh J, George JC, Botta O, Zauscher M, Bada JL, O'Hara TM (2012) Age estimates based on aspartic acid racemization for bowhead whales (Balaena mysticetus) harvested in 1998-2000 and the relationship between racemization rate and body temperature. Marine Mammal Science, 29, 424-445.
70. Schippers A, Neretin L, Kallmeyer J, Ferdelman T, Cragg B, Parkes R, Jørgensen B (2005) Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861-864.
71. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriological Reviews 36, 407-477.
72. Scholten JCM, Conrad R (2000) Energetics of syntrophic propionate oxidation in defined batch and chemostat cocultures. Applied and Environmental Microbiology 66, 2934-2942.
73. Staudenbauer W (1968) D-aspartic acid incorporation into interpeptide bridges in bacterial cell wall. Federation Proceedings 27, 294.
74. Stetter KO, Huber R, Blochl E, Kurr M, Eden RD, Fielder M, Cash H, Vance I (1993) Hyperthermophilic Archaea are thriving in deep North-Sea and Alaskan oil-reservoirs. Nature 365, 743-745.
75. Stouthamer AH (1979) The search for correlation between theoretical and experimental growth yields. In Microbial Biochemistry (ed Quayle JR). University Park Press, Baltimore, MD, pp. 1-47.
76. Takahata Y, Hoaki T, Maruyama T (2001) Starvation survivability of Thermococcus strains isolated from Japanese oil reservoirs. Archives of Microbiology 176, 264-270.
77. Takai K, Moser DP, DeFlaun MF, Onstott TC, Fredrickson JK (2001) Archaeal diversity in waters from deep South African Gold mines. Applied and Environmental Microbiology 67, 5750-5760.
78. 4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proceedings of the National Academy of Sciences of the USA 105, 10949-10954.
79. Takano Y, Sato R, Kaneko T, Kobayashi K, Marumo K (2003) Biological origin for amino acids in a deep subterranean hydrothermal vent, Toyoha mine, Hokkaido, Japan. Organic Geochemistry 34, 1491-1496.
80. Tijhuis L, vanLoosdrecht MCM, Heijnen JJ (1993) A thermodynamically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnology and Bioengineering 42, 509-519.
81. Tomizawa H, Yamada H, Wada K, Imoto T (1995) Stabilization of lysozyme against irreversible inactivation by suppression of chemical reactions. Journal of Biochemistry 117, 635-640.
82. VerEecke HC, Butterfield DA, Huber JA, Lilley MD, Olsond EJ, Roe KK, Evans LJ, Merkel AY, Cantin HV, Holden JF (2012) Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents. Proceedings of the National Academy of Sciences of the USA 109, 13674-13679.
83. Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiology and Molecular Biology Reviews 65, 1-43.
84. van de Vossenberg JLCM, Ubbink-Kok T, Elferink MGL, Driessen AJM, Konings WN (1995) Ion permeability of the cytoplasmic membrane limits the maximum growth temperature of bacteria and archaea. Molecular Microbiology, 18, 925-932.
85. van derWal A, Norde W, Bendinger B, Zehnder AJB, Lyklema J (1997) Chemical analysis of isolated cell walls of Gram-positive bacteria and determination of the cell wall to cell mass ratio. Journal of Microbiological Methods 28, 147-157.
86. Ward JA, Slater GF, Moser DP, Lin L-H, Lacrampe-Couloume G, Bonin AP, Davidson M, Hall JA, Mislowack B, Bellamy RES, Onstott TC, Sherwood Lollar B (2004) Microbial hydrocarbon gases in the witwatersrand basin, south africa: implications for the deep biosphere. Geochimica et Cosmochimica Acta 68, 3239-3250.
87. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proceedings of the National Academy of Sciences of the USA 95, 6578-6583.
88. Wilhelms A, Larter SR, Head I, Farrimond P, di-Primio R, Zwach C (2001) Biodegradation of oil in uplifted basins prevented by deep-burial sterilization. Nature 411, 1034-1037.
89. Willey JM, Sherwood LM, Woolverton CJ (2011) Prescott's Microbiology. McGraw-Hill Education, New York, NY, 1012100101.
90. Yamauchi T, Choi S-Y, Oikada H, Yohda M, Kumagai H, Esaki N, Soda K (1992) Properties of aspartate racemase, a pyridoxal 5′-phosphate-independent amino acid racemase. Journal of Biological Chemistry, 267, 18361-18364.
91. Zhao M, Bada JL (1995) Determination of α-dialkylamino acids and their enantiomers in geological samples by high-performance liquid chromatography after derivatization with a chiral adduct of o-phthaldialdehyde. Journal of Chromatography A 690, 55-63.