Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone

PeerJ

Volumn 2016, Issue 11, 2016, Pages

  Butterfield, Cristina N ^a   Li, Zhou ^b   Andeer, Peter F ^c   Spaulding, Susan ^a   Thomas, Brian C ^a   Singh, Andrea ^a   Hettich, Robert L ^b   Suttle, Kenwyn B ^d   Probst, Alexander J ^a   Tringe, Susannah G ^e   Northen, Trent ^c   Pan, Chongle ^b   Banfield, Jillian F ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e DOE JOINT GENOME INSTITUTE   (United States)

Author keywords

Genome resolved metagenomics; Metabolomics; Methanol dehydrogenase; Proteomics; Soil archaea; Soil bacteria

Indexed keywords

AMINO ACID; METHANOL;

ARCHAEON; ARTICLE; BACTERIUM; CLIMATE; GEMMATIMONADETES; GENOMICS; GRASS; GRASSLAND; METABOLITE; METAGENOME; METHYLOTROPH; MICROBIAL COMMUNITY; NONHUMAN; NUTRIENT AVAILABILITY; PLANT ROOT; PROTEIN DEGRADATION; PROTEOMICS; RHIZOSPHERE; SOIL MICROFLORA; TURNOVER TIME;

EID: 84995468063     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.2687     Document Type: Article

References (99)

1. Aanderud ZT, Jones SE, Schoolmaster DR, Fierer N, Lennon JT. 2013. Sensitivity of soil respiration and microbial communities to altered snowfall. Soil Biology and Biochemistry 57:217-227 DOI 10.1016/j.soilbio.2012.07.022.
2. Adair KL, Wratten S, Lear G. 2013. Soil phosphorus depletion and shifts in plant com-munities change bacterial community structure in a long-term grassland manage-ment trial. Environmental Microbiology Reports 5:404-413 DOI 10.1111/1758-2229.12049.
3. Aerts R, Bakker C, De Caluwe H. 1992. Root turnover as determinant of the cy-cling of C, N, and P in a dry heathland ecosystem. Biogeochemistry 15:175-190 DOI 10.1007/BF00002935.
4. Anthony C, Williams P. 2003. The structure and mechanism of methanol dehy-drogenase. Biochimica et Biophysica Acta-Proteins and Proteomics 1647:18-23 DOI 10.1016/S1570-9639(03)00042-6.
5. Banning NC, Gleeson DB, Grigg AH, Grant CD, Andersen GL, Brodie EL, Murphy DV. 2011. Soil microbial community successional patterns during forest ecosystem restoration. Applied and Environmental Microbiology 77:6158-6164 DOI 10.1128/AEM.00764-11.
6. Beck DAC, McTaggart TL, Setboonsarng U, Vorobev A, Kalyuzhnaya MG, Ivanova N, Goodwin L, Woyke T, Lidstrom ME, Chistoserdova L. 2014. The ex-panded diversity of Methylophilaceae from Lake Washington through cul-tivation and genomic sequencing of novel ecotypes. PLoS ONE 9:e102458 DOI 10.1371/journal.pone.0102458.
7. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57:289-300.
8. Berendse F. 1994. Litter decomposability-a neglected component of plant fitness. Journal of Ecology 82:187-190 DOI 10.2307/2261398.
9. Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB, Anderson R, Fredricks HF, Elvert M, Kelly TJ, Schrag DP, Sogin ML, Brenchley JE, Teske A, House CH, Hinrichs K-U. 2006. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proceedings of the National Academy of Sciences of the United States of America 103:3846-3851 DOI 10.1073/pnas.0600035103.
10. Blazewicz SJ, Schwartz E, Firestone MK. 2014. Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil. Ecology 95:1162-1172 DOI 10.1890/13-1031.1.
11. Bogart JA, Lewis AJ, Schelter EJ. 2015. DFT study of the active site of the XoxF-type nat-ural, cerium-dependent methanol dehydrogenase enzyme. Chemistry 21:1743-1748 DOI 10.1002/chem.201405159.
12. Brooks B, Mueller RS, Young JC, Morowitz MJ, Hettich RL, Banfield JF. 2015. Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant. Frontiers in Microbiology 6: Article 654 DOI 10.3389/fmicb.2015.00654.
13. Castelle CJ, Wrighton KC, Thomas BC, Hug LA, Brown CT, Wilkins MJ, Frischkorn KR, Tringe SG, Singh A, Markillie LM, Taylor RC, Williams KH, Banfield JF. 2015. Genomic expansion of domain archaea highlights roles for organ-isms from new phyla in anaerobic carbon cycling. Current Biology 25:690-701 DOI 10.1016/j.cub.2015.01.014.
14. Chistoserdova L. 2011. Modularity of methylotrophy, revisited. Environmental Microbiology 13:2603-2622 DOI 10.1111/j.1462-2920.2011.02464.x.
15. Corpe WA, Rheem S. 1989. Ecology of the methylotrophic bacteria on living leaf sur-faces. FEMS Microbiology Letters 62:243-249 DOI 10.1016/0378-1097(89)90248-6.
16. Costello AM, Lidstrom ME. 1999. Molecular characterization of functional and phylo-genetic genes from natural populations of methanotrophs in lake sediments. Applied and Environmental Microbiology 65:5066-5074.
17. Cruz-Martínez K, Suttle KB, Brodie EL, Power ME, Andersen GL, Banfield JF. 2009. Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME Journal 3:738-744 DOI 10.1038/ismej.2009.16.
18. Delmont TO, Eren AM, Maccario L, Prestat E, Esen OC, Pelletier E, Le Paslier D, Simonet P, Vogel TM. 2015. Reconstructing rare soil microbial genomes using in situ enrichments and metagenomics. Frontiers in Microbiology 6: Article 358 DOI 10.3389/fmicb.2015.00358.
19. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, Von Mering C, Vorholt JA. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proceedings of the National Academy of Sciences of the United States of America 106:16428-16433 DOI 10.1073/pnas.0905240106.
20. Dixon P. 2003. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14:927-930.
21. Edgar R. 2004a. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:1-19 DOI 10.1186/1471-2105-5-113.
22. Edgar RC. 2004b. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792-1797 DOI 10.1093/nar/gkh340.
23. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461 DOI 10.1093/bioinformatics/btq461.
24. Elias JE, Gygi SP. 2007. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nature Methods 4:207-214 DOI 10.1038/nmeth1019.
25. Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW. 2015. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350:434-438 DOI 10.1126/science.aac7745.
26. Evans SE, Wallenstein MD. 2012. Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101-116 DOI 10.1007/s10533-011-9638-3.
27. Eyice O, Namura M, Chen Y, Mead A, Samavedam S, Schafer H. 2015. SIP metage-nomics identifies uncultivated Methylophilaceae as dimethylsulphide degrading bac-teria in soil and lake sediment. ISME Journal 9:2336-2348 DOI 10.1038/ismej.2015.37.
28. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG. 2012. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proceedings of the National Academy of Sciences of the United States of America 109:21390-21395 DOI 10.1073/pnas.1215210110.
29. Fischer H, Ingwersen J, Kuzyakov Y. 2010. Microbial uptake of low-molecular-weight organic substances out-competes sorption in soil. European Journal of Soil Science 61:504-513 DOI 10.1111/j.1365-2389.2010.01244.x.
30. Gagen EJ, Huber H, Meador T, Hinrichs KU, Thomm M. 2013. Novel cultivation-based approach to understanding the Miscellaneous Crenarchaeotic Group (MCG) archaea from sedimentary ecosystems. Applied and Environmental Microbiology 79:6400-6406 DOI 10.1128/AEM.02153-13.
31. Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL. 2011. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Frontiers in Microbiology 2: Article 94 DOI 10.3389/fmicb.2011.00094.
32. He J, Xu Z, Hughes J. 2006. Molecular bacterial diversity of a forest soil under residue management regimes in subtropical Australia. FEMS Microbiology Ecology 55:38-47 DOI 10.1111/j.1574-6941.2005.00006.x.
33. Henckel T, Friedrich M, Conrad R. 1999. Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Applied and Environmental Microbiology 65:1980-1990.
34. Herzberger AJ, Duncan DS, Jackson RD. 2014. Bouncing back: plant-associated soil microbes respond rapidly to prairie establishment. PLoS ONE 9:e115775 DOI 10.1371/journal.pone.0115775.
35. Hofmann K, Pauli H, Praeg N, Wagner AO, Illmer P. 2016. Methane-cycling microor-ganisms in soils of a high-alpine altitudinal gradient. FEMS Microbiology Ecology 92(3): fiw009 DOI 10.1093/femsec/fiw009.
36. Hug LA, Thomas BC, Brown CT, Frischkorn KR, Williams KH, Tringe SG, Banfield JF. 2015. Aquifer environment selects for microbial species cohorts in sediment and groundwater. ISME Journal 9:1846-1856 DOI 10.1038/ismej.2015.2.
37. Hug LA, Thomas BC, Sharon I, Brown CT, Sharma R, Hettich RL, Wilkins MJ, Williams KH, Singh A, Banfield JF. 2016. Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages. Environmental Microbiology 18:159-173 DOI 10.1111/1462-2920.12930.
38. Hultman J, Waldrop MP, Mackelprang R, David MM, McFarland J, Blazewicz SJ, Harden J, Turetsky MR, McGuire AD, Shah MB, VerBerkmoes NC, Lee LH, Mavrommatis K, Jansson JK. 2015. Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521:208-212 DOI 10.1038/nature14238.
39. Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119 DOI 10.1186/1471-2105-11-119.
40. Hyatt D, Pan C. 2012. Exhaustive database searching for amino acid mutations in proteomes. Bioinformatics 28:1895-1901 DOI 10.1093/bioinformatics/bts274.
41. Jones DL, Shannon D, Murphy DV, Farrar J. 2004. Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biology and Biochemistry 36:749-756 DOI 10.1016/j.soilbio.2004.01.003.
42. Kandeler E, Mosier AR, Morgan JA, Milchunas DG, King JY, Rudolph S, Tscherko D. 2006. Response of soil microbial biomass and enzyme activities to the transient elevation of carbon dioxide in a semi-arid grassland. Soil Biology and Biochemistry 38:2448-2460 DOI 10.1016/j.soilbio.2006.02.021.
43. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research 40:D109-D114 DOI 10.1093/nar/gkr988.
44. Karl DM, Beversdorf L, Bjorkman KM, Church MJ, Martinez A, Delong EF. 2008. Aerobic production of methane in the sea. Nature Geoscience 1:473-478 DOI 10.1038/ngeo234.
45. Keltjens JT, Pol A, Reimann J, Op Den Camp HJM. 2014. PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference. Applied Microbiology and Biotechnology 98:6163-6183 DOI 10.1007/s00253-014-5766-8.
46. Kolb S. 2009. Aerobic methanol-oxidizing Bacteria in soil. FEMS Microbiology Letters 300:1-10 DOI 10.1111/j.1574-6968.2009.01681.x.
47. Kubo K, Lloyd KG, Biddle JF, Amann R, Teske A, Knittel K. 2012. Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME Journal 6:1949-1965 DOI 10.1038/ismej.2012.37.
48. Kuramae EE, Yergeau E, Wong LC, Pijl AS, Van Veen JA, Kowalchuk GA. 2012. Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiology Ecology 79:12-24 DOI 10.1111/j.1574-6941.2011.01192.x.
49. Lauber CL, Hamady M, Knight R, Fierer N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology 75:5111-5120 DOI 10.1128/AEM.00335-09.
50. Li Z, Wang Y, Yao Q, Justice NB, Ahn TH, Xu D, Hettich RL, Banfield JF, Pan C. 2014. Diverse and divergent protein post-translational modifications in two growth stages of a natural microbial community. Nature Communications 5: Article 4405 DOI 10.1038/ncomms5405.
51. Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stepanauskas R, Richter M, Kleindienst S, Lenk S, Schramm A, Jorgensen BB. 2013. Predominant archaea in marine sediments degrade detrital proteins. Nature 496:215-218 DOI 10.1038/nature12033.
52. Luo C, Rodriguez-R LM, Johnston ER, Wu L, Cheng L, Xue K, Tu Q, Deng Y, He Z, Shi JZ, Yuan MM, Sherry RA, Li D, Luo Y, Schuur EAG, Chain P, Tiedje JM, Zhou J, Konstantinidis KT. 2014. Soil microbial community responses to a decade of warming as revealed by comparative metagenomics. Applied and Environmental Microbiology 80:1777-1786 DOI 10.1128/AEM.03712-13.
53. Markham P, Robson GD, Bainbridge BW, Trinci AP. 1993. Choline: its role in the growth of filamentous fungi and the regulation of mycelial morphology. FEMS Microbiology Reviews 10:287-300.
54. Mau RL, Liu CM, Aziz M, Schwartz E, Dijkstra P, Marks JC, Price LB, Keim P, Hungate BA. 2015. Linking soil bacterial biodiversity and soil carbon stability. ISME Journal 9:1477-1480 DOI 10.1038/ismej.2014.205.
55. McKissock I, Gilkes RJ, Walker EL. 2002. The reduction of water repellency by added clay is influenced by clay and soil properties. Applied Clay Science 20:225-241 DOI 10.1016/S0169-1317(01)00074-6.
56. Metcalf WW, Griffin BM, Cicchillo RM, Gao J, Janga SC, Cooke HA, Circello BT, Evans BS, Martens-Habbena W, Stahl DA, Van der Donk WA. 2012. Synthesis of methylphosphonic acid by marine microbes: a source for methane in the aerobic ocean. Science 337:1104-1107 DOI 10.1126/science.1219875.
57. Mosier AC, Li Z, Thomas BC, Hettich RL, Pan C, Banfield JF. 2015. Elevated tempera-ture alters proteomic responses of individual organisms within a biofilm community. ISME Journal 9:180-194 DOI 10.1038/ismej.2014.113.
58. Muyzer G, De Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59:695-700.
59. Nawrocki EP, Kolbe DL, Eddy SR. 2009. Infernal 1.0: inference of RNA alignments. Bioinformatics 25:1335-1337 DOI 10.1093/bioinformatics/btp157.
60. Nercessian O, Noyes E, Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L. 2005. Bacterial populations active in metabolism of C1 compounds in the sediment of Lake Washington, a freshwater lake. Applied and Environmental Microbiology 71:6885-6899 DOI 10.1128/AEM.71.11.6885-6899.2005.
61. Nesvizhskii AI, Aebersold R. 2005. Interpretation of shotgun proteomic data: the protein inference problem. Molecular & Cellular Proteomics 4:1419-1440 DOI 10.1074/mcp.R500012-MCP200.
62. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. 1999. KEGG: ky-oto encyclopedia of genes and genomes. Nucleic Acids Research 27:29-34 DOI 10.1093/nar/27.1.29.
63. Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A, Schouten S, Jetten MSM, Birkeland NK, Pol A, Dunfield PF. 2009. Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environmental Microbiology Reports 1:293-306 DOI 10.1111/j.1758-2229.2009.00022.x.
64. Osborn AM, Moore ERB, Timmis KN. 2000. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environmental Microbiology 2:39-50 DOI 10.1046/j.1462-2920.2000.00081.x.
65. Pan C, Banfield JF. 2014. Quantitative metaproteomics: functional insights into micro-bial communities. Methods in Molecular Biology 1096:231-240 DOI 10.1007/978-1-62703-712-9_18.
66. Pell J, Hintze A, Canino-Koning R, Howe A, Tiedje JM, Brown CT. 2012. Scaling metagenome sequence assembly with probabilistic de Bruijn graphs. Proceedings of the National Academy of Sciences of the United States of America 109:13272-13277 DOI 10.1073/pnas.1121464109.
67. Peltoniemi K, Laiho R, Juottonen H, Kiikkilä O, Mäkiranta P, Minkkinen K, Pennanen T, Penttilä T, Sarjala T, Tuittila E-S, Tuomivirta T, Fritze H. 2015. Microbial ecology in a future climate: effects of temperature and moisture on microbial communities of two boreal fens. FEMS Microbiology Ecology 91(7): fiv062 DOI 10.1093/femsec/fiv062.
68. Peng Y, Leung HCM, Yiu SM, Chin FYL. 2012. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28:1420-1428 DOI 10.1093/bioinformatics/bts174.
69. Pester M, Rattei T, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M. 2012. AmoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environmental Microbiology 14:525-539 DOI 10.1111/j.1462-2920.2011.02666.x.
70. Piper CL, Siciliano SD, Winsley T, Lamb EG. 2015. Smooth brome invasion increases rare soil bacterial species prevalence, bacterial species richness and evenness. Journal of Ecology 103:386-396 DOI 10.1111/1365-2745.12356.
71. Placella SA, Brodie EL, Firestone MK. 2012. Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proceedings of the National Academy of Sciences of the United States of America 109:10931-10936 DOI 10.1073/pnas.1204306109.
72. Pol A, Barends TRM, Dietl A, Khadem AF, Eygensteyn J, Jetten MSM, Op den Camp HJM. 2014. Rare earth metals are essential for methanotrophic life in volcanic mudpots. Environmental Microbiology 16:255-264 DOI 10.1111/1462-2920.12249.
73. Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, Lind EM, Seabloom EW, Adler PB, Bakker JD, Cleland EE, Decrappeo NM, Delorenze E, Hagenah N, Hautier Y, Hofmockel KS, Kirkman KP, Knops JMH, La Pierre KJ, Macdougall AS, McCulley RL, Mitchell CE, Risch AC, Schuetz M, Stevens CJ, Williams RJ, Fierer N. 2015. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecology Letters 18:85-95 DOI 10.1111/ele.12381.
74. 2 concentrations. Environmental Microbiology Epub ahead of print Apr 26 2016 DOI 10.1111/1462-2920.13362.
75. Pruesse E, Peplies J, Glöckner FO. 2012. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823-1829 DOI 10.1093/bioinformatics/bts252.
76. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research 35:7188-7196 DOI 10.1093/nar/gkm864.
77. Radajewski S, Webster G, Reay DS, Morris SA, Ineson P, Nedwell DB, Prosser JI, Murrell JC. 2002. Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiology 148:2331-2342.
78. R Core Team. 2015. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at http://www.R-project.org/.
79. Reinsch S, Michelsen A, Sárossy Z, Egsgaard H, Schmidt IK, Jakobsen I, Ambus P. 2014. Short-term utilization of carbon by the soil microbial community under future climatic conditions in a temperate heathland. Soil Biology and Biochemistry 68:9-19 DOI 10.1016/j.soilbio.2013.09.014.
80. Schimel JP, Schaeffer SM. 2012. Microbial control over carbon cycling in soil. Frontiers in Microbiology 3: Article 348 DOI 10.3389/fmicb.2012.00348.
81. Scott JW, Rasche ME. 2002. Purification, overproduction, and partial characterization of β-RFAP synthase, a key enzyme in the methanopterin biosynthesis pathway. Journal of Bacteriology 184:4442-4448 DOI 10.1128/jb.184.16.4442-4448.2002.
82. Sharon I, Kertesz M, Hug LA, Pushkarev D, Blauwkamp TA, Castelle CJ, Amirebrahimi M, Thomas BC, Burstein D, Tringe SG, Williams KH, Banfield JF. 2015. Accurate, multi-kb reads resolve complex populations and detect rare microorganisms. Genome Research 25:534-543 DOI 10.1101/gr.183012.114.
83. Skovran E, Gomez NCM. 2015. Just add lanthanides. Science 348:862-863 DOI 10.1126/science.aaa9091.
84. Stacheter A, Noll M, Lee CK, Selzer M, Glowik B, Ebertsch L, Mertel R, Schulz D, Lampert N, Drake HL, Kolb S. 2013. Methanol oxidation by temperate soils and en-vironmental determinants of associated methylotrophs. ISME Journal 7:1051-1064 DOI 10.1038/ismej.2012.167.
85. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313 DOI 10.1093/bioinformatics/btu033.
86. Suttle KB, Thomsen MA, Power ME. 2007. Species interactions reverse grassland responses to changing climate. Science 315:640-642 DOI 10.1126/science.1136401.
87. Sutton R, Sposito G. 2005. Molecular structure in soil humic substances: the new view. Environmental Science and Technology 39:9009-9015 DOI 10.1021/es050778q.
88. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH. 2007. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23:1282-1288 DOI 10.1093/bioinformatics/btm098.
89. Swenson TL, Jenkins S, Bowen BP, Northen TR. 2015. Untargeted soil metabolomics methods for analysis of extractable organic matter. Soil Biology and Biochemistry 80:189-198 DOI 10.1016/j.soilbio.2014.10.007.
90. Taubert M, Grob C, Howat AM, Burns OJ, Dixon JL, Chen Y, Murrell JC. 2015. XoxF encoding an alternative methanol dehydrogenase is widespread in coastal marine environments. Environmental Microbiology 17:3937-3948 DOI 10.1111/1462-2920.12896.
91. Verastegui Y, Cheng J, Engel K, Kolczynski D, Mortimer S, Lavigne J, Montalibet J, Romantsov T, Hall M, McConkey BJ, Rose DR, Tomashek JJ, Scott BR, Charles TC, Neufeld JD. 2014. Multisubstrate isotope labeling and metagenomic analysis of active soil bacterial communities. mBio 5:e44203 DOI 10.1128/mBio.01157-14.
92. Veresoglou SD, Thornton B, Menexes G, Mamolos AP, Veresoglou DS. 2012. Soil fertilization leads to a decline in between-samples variability of microbial com-munity δ13C profiles in a grassland fertilization experiment. PLoS ONE 7:e44203 DOI 10.1371/journal.pone.0044203.
93. Vizcaíno JA, Csordas A, Del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T, Xu QW, Wang R, Hermjakob H. 2016. 2016 update of the PRIDE database and its related tools. Nucleic Acids Research 44:D447-D456 DOI 10.1093/nar/gkv1145.
94. Wang Y, Ahn TH, Li Z, Pan C. 2013. Sipros/ProRata: a versatile informatics sys-tem for quantitative community proteomics. Bioinformatics 29:2064-2065 DOI 10.1093/bioinformatics/btt329.
95. Washburn MP, Wolters D, Yates 3rd JR. 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nature Biotechnology 19:242-247 DOI 10.1038/85686.
96. Wedin DA, Tilman D. 1990. Species effects on nitrogen cycling: a test with perennial grasses. Oecologia 84:433-441 DOI 10.1007/BF00328157.
97. White RA, Bottos EM, Roy Chowdhury T, Zucker JD, Brislawn CJ, Nicora CD, Fansler SJ, Glaesemann KR, Glass K, Jansson JK. 2016. Moleculo long-read sequencing facilitates assembly and genomic binning from complex soil metagenomes. mSystems 1(3):e00045-16 DOI 10.1128/mSystems.00045-16.
98. White R, Murray A, Rohweder M. 2000. Pilot analysis of global ecosystems: grassland ecosystems. Washington, D.C.: World Resources Institute.
99. Wisniewski JR, Zougman A, Nagaraj N, Mann M. 2009. Universal sample preparation method for proteome analysis. Nature Methods 6:359-362 DOI 10.1038/nmeth.1322.