15N- and 2H proteomic stable isotope probing links nitrogen flow to archaeal heterotrophic activity

Environmental Microbiology

Volumn 16, Issue 10, 2014, Pages 3224-3237

  Justice, Nicholas B ^a,c   Li, Zhou ^b   Wang, Yingfeng ^b   Spaudling, Susan E ^a   Mosier, Annika C ^a   Hettich, Robert L ^b   Pan, Chongle ^b   Banfield, Jillian F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA;

ARCHAEAL PROTEIN; BACTERIAL PROTEIN; DEUTERIUM OXIDE; IRON; NITROGEN;

ARCHAEON; BACTERIA; BIOFILM; BIOSYNTHESIS; ECOSYSTEM; HETEROTROPHY; METABOLISM; OXIDATION REDUCTION REACTION; PROTEOMICS;

ARCHAEA; ARCHAEAL PROTEINS; BACTERIA; BACTERIAL PROTEINS; BIOFILMS; DEUTERIUM OXIDE; ECOSYSTEM; HETEROTROPHIC PROCESSES; IRON; NITROGEN; NITROGEN ISOTOPES; OXIDATION-REDUCTION; PROTEOMICS;

EID: 84907881942     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12488     Document Type: Article

References (47)

1. Aliaga Goltsman, D.S., Dasari, M., Thomas, B.C., Shah, M.B., VerBerkmoes, N.C., Hettich, R.L., etal. (2013) A new group in the Leptospirillum clade: cultivation-independent community genomics, proteomics and transcriptomics of the new species Leptospirillum group IV UBA BS. Appl Environ Microbiol 79: 5384-5393.
2. Baker, B.J., Tyson, G.W., Goosherst, L., and Banfield, J.F. (2009) Insights into the diversity of eukaryotes in acid mine drainage biofilm communities. Appl Environ Microbiol 75: 2192-2199.
3. Belnap, C.P., Pan, C., VerBerkmoes, N.C., Power, M.E., Samatova, N.F., Carver, R.L., etal. (2009) Cultivation and quantitative proteomic analyses of acidophilic microbial communities. ISME J 4: 520-530.
4. Belnap, C.P., Pan, C., Denef, V.J., Samatova, N.F., Hettich, R.L., and Banfield, J.F. (2011) Quantitative proteomic analyses of the response of acidophilic microbial communities to different pH conditions. ISME J 5: 1152-1161.
5. Boschker, H.T.S., Nold, S.C., Wellsbury, P., Bos, D., de Graaf, W., Pel, R., etal. (1998) Direct linking of microbial populations to specific biogeochemical processes by 13C-labelling of biomarkers. Nature 392: 801-805.
6. Bridge, T., and Johnson, D. (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.
7. Chourey, K., Jansson, J., VerBerkmoes, N., Shah, M., Chavarria, K.L., Tom, L.M., etal. (2010) Direct cellular lysis/protein extraction protocol for soil metaproteomics. J Proteome Res 9: 6615-6622.
8. Denef, V.J., and Banfield, J.F. (2012) In situ evolutionary rate measurements show ecological success of recently emerged bacterial hybrids. Science 336: 462-466.
9. Denef, V.J., Mueller, R.S., and Banfield, J.F. (2010) AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4: 599-610.
10. Dick, G.J., Andersson, A.F., Baker, B.J., Simmons, S.L., Thomas, B.C., Yelton, A.P., etal. (2009) Community-wide analysis of microbial genome sequence signatures. Genome Biol 10: R85.
11. Dopson, M., Baker-Austin, C., and Bond, P. (2006) Towards determining details of anaerobic growth coupled to ferric iron reduction by the acidophilic archaeon 'Ferroplasma acidarmanus' Fer1. Extremophiles 11: 159-168.
12. Druschel, G.K., Baker, B.J., Gihring, T.M., and Banfield, J.F. (2004) Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem Trans 5: 13-32.
13. Dumont, M.G., and Murrell, J.C. (2005) Stable isotope probing - linking microbial identity to function. Nat Rev Microbiol 3: 499-504.
14. Fetzer, I., Jehmlich, N., Vogt, C., Richnow, H.-H., Seifert, J., Harms, H., etal. (2010) Calculation of partial isotope incorporation into peptides measured by mass spectrometry. BMC Res Notes 3: 178.
15. Giovanni, R. (1961) The effects of deuterium oxide on bacteria. Z Vererbungsl 92: 389-402.
16. Giovanni, R. (1963) Studies on incorporation of deuterium into bacteria. Biochem J 87: 79-82.
17. Goltsman, D.S.A., Denef, V.J., Singer, S.W., VerBerkmoes, N.C., Lefsrud, M., Mueller, R.S., etal. (2009) Community genomic and proteomic analyses of chemoautotrophic iron-oxidizing 'Leptospirillum rubarum' (Group II) and 'Leptospirillum ferrodiazotrophum' (Group III) bacteria in acid mine drainage biofilms. Appl Environ Microbiol 75: 4599-4615.
18. Gutierrez-Zamora, M.-L., and Manefield, M. (2010) An appraisal of methods for linking environmental processes to specific microbial taxa. Rev Environ Sci Biotechnol 9: 153-185.
19. Hoch, M.P., and Kirchman, D.L. (1995) Ammonium uptake by heterotrophic bacteria in the Delaware estuary and adjacent coastal waters. Limnol Oceanogr 40: 886-897.
20. Jehmlich, N., Schmidt, F., von Bergen, M., Richnow, H.-H., and Vogt, C. (2008a) Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures. ISME J 2: 1122-1133.
21. Jehmlich, N., Schmidt, F., Hartwich, M., von Bergen, M., Richnow, H.-H., and Vogt, C. (2008b) Incorporation of carbon and nitrogen atoms into proteins measured by protein-based stable isotope probing (Protein-SIP). Rapid Commun Mass Spectrom 22: 2889-2897.
22. Jehmlich, N., Fetzer, I., Seifert, J., Mattow, J., Vogt, C., Harms, H., etal. (2010a) Decimal place slope, a fast and precise method for quantifying 13C incorporation levels for detecting the metabolic activity of microbial species. Mol Cell Proteomics 9: 1221-1227.
23. Jehmlich, N., Schmidt, F., Taubert, M., Seifert, J., Bastida, F., von Bergen, M., etal. (2010b) Protein-based stable isotope probing. Nat Protoc 5: 1957-1966.
24. Johnson, D.B., Joulian, C., d'Hugues, P., and Hallberg, K.B. (2008) Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations. Extremophiles 12: 789-798.
25. Justice, N.B., Pan, C., Mueller, R., Spaulding, S.E., Shah, V., Sun, C.L., etal. (2012) Heterotrophic archaea contribute to carbon cycling in low-pH, suboxic biofilm communities. Appl Environ Microbiol 78: 8321-8330.
26. Lo, I., Denef, V.J., VerBerkmoes, N.C., Shah, M.B., Goltsman, D., DiBartolo, G., etal. (2007) Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446: 537-541.
27. Muller, J., Szklarczyk, D., Julien, P., Letunic, I., Roth, A., Kuhn, M., etal. (2010) eggNOG v2.0: extending the evolutionary genealogy of genes with enhanced non-supervised orthologous groups, species and functional annotations. Nucleic Acids Res 38: D190-D195.
28. Northrop, D.B. (1975) Steady-state analysis of kinetic isotope effects in enzymic reactions. Biochemistry 14: 2644-2651.
29. Pan, C.L., Fischer, C.R., Hyatt, D., Bowen, B.P., Hettich, R.L., and Banfield, J.F. (2011) Quantitative tracking of isotope flows in proteomes of microbial communities. Mol Cell Proteomics 10: M110-M6049.
30. Peng, J., Elias, J.E., Thoreen, C.C., Licklider, L.J., and Gygi, S.P. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2: 43-50.
31. Radajewski, S., Ineson, P., Parekh, N.R., and Murrell, J.C. (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403: 646-649.
32. Singer, S.W., Chan, C.S., Zemla, A., VerBerkmoes, N.C., Hwang, M., Hettich, R.L., etal. (2008) Characterization of cytochrome 579, an unusual cytochrome isolated from an iron-oxidizing microbial community. Appl Environ Microbiol 74: 4454-4462.
33. Singer, S.W., Erickson, B.K., VerBerkmoes, N.C., Hwang, M., Shah, M.B., Hettich, R.L., etal. (2010) Posttranslational modification and sequence variation of redox-active proteins correlate with biofilm life cycle in natural microbial communities. ISME J 4: 1398-1409.
34. Stookey, L.L. (1970) Ferrozine - a new spectrophotometric reagent for iron. Anal Chem 42: 779-781.
35. Taubert, M., Baumann, S., von Bergen, M., and Seifert, J. (2011) Exploring the limits of robust detection of incorporation of 13C by mass spectrometry in protein-based stable isotope probing (protein-SIP). Anal Bioanal Chem 401: 1975-1982.
36. Taubert, M., Vogt, C., Wubet, T., Kleinsteuber, S., Tarkka, M.T., Harms, H., etal. (2012) Protein-SIP enables time-resolved analysis of the carbon flux in a sulfate-reducing, benzene-degrading microbial consortium. ISME J 6: 2291-2301.
37. Taubert, M., Bergen, M., and Seifert, J. (2013) Limitations in detection of 15N incorporation by mass spectrometry in protein-based stable isotope probing (protein-SIP). Anal Bioanal Chem 405: 3989-3996.
38. Thomson, J.F. (1963) Biological Effects of Deuterium. Oxford, UK: Pergamon Press.
39. Tsaplina, I.A., Zhuravleva, A.E., Egorova, M.A., Bogdanova, T.I., Krasil'nikova, E.N., Zakharchuk, L.M., etal. (2010) Response to oxygen limitation in bacteria of the genus Sulfobacillus. Microbiology 79: 13-22.
40. Tyson, G.W., Chapman, J., Hugenholtz, P., Allen, E.E., Ram, R.J., Richardson, P.M., etal. (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37-43.
41. Uhlík, O., Jecná, K., Leigh, M.B., Macková, M., and Macek, T. (2009) DNA-based stable isotope probing: a link between community structure and function. Sci Total Environ 407: 3611-3619.
42. Wade, D. (1999) Deuterium isotope effects on noncovalent interactions between molecules. Chem Biol Interact 117: 191-217.
43. Wang, Y., Ahn, T.H., Li, Z., and Pan, C. (2013) Sipros/ProRata: a versatile informatics system for quantitative community proteomics. Bioinformatics 29: 2064-2065.
44. Washburn, M.P., Wolters, D., and Yates, J.R. (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247.
45. Wood, A.P., and Kelly, D.P. (1984) Growth and sugar metabolism of a thermoaddophilic iron-oxidizing mixotrophic bacterium. Microbiology 130: 1337-1349.
46. Yelton, A.P., Comolli, L.R., Justice, N.B., Castelle, C., Denef, V.J., Thomas, B.C., and Banfield, J.F. (2013) Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea. BMC Genomics 14: 485.
47. Ziegler, S., Dolch, K., Geiger, K., Krause, S., Asskamp, M., Eusterhues, K., etal. (2013) Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria. ISME J 7: 1725-1737.