Soil microbial community responses to a decade of warming as revealed by comparative metagenomics

Applied and Environmental Microbiology

Volumn 80, Issue 5, 2014, Pages 1777-1786

  Luo, Chengwei ^a   Rodriguez R, Luis M ^a   Johnston, Eric R ^h   Wu, Liyou ^b   Cheng, Lei ^b   Xue, Kai ^b   Tu, Qichao ^b   Deng, Ye ^b   He, Zhili ^b   Shi, Jason Zhou ^b   Yuan, Mengting Maggie ^b   Sherry, Rebecca A ^b   Li, Dejun ^b   Luo, Yiqi ^b   Schuur, Edward A G ^c   Chain, Patrick ^d   Tiedje, James M ^e   Zhou, Jizhong ^b,f,g   Konstantinidis, Konstantinos T ^a,h  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

^f LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^g TSINGHUA UNIVERSITY   (China)

^h Georgia Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; NITROGEN;

ARTICLE; BIOTA; GREENHOUSE EFFECT; HUMAN; METABOLISM; METAGENOMICS; MICROBIOLOGY; RADIATION EXPOSURE; UNITED STATES;

BIOTA; CARBON; GLOBAL WARMING; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METAGENOMICS; MIDWESTERN UNITED STATES; NITROGEN; SOIL MICROBIOLOGY;

EID: 84894050299     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03712-13     Document Type: Article

References (55)

1. Allison SD, Martiny JB. 2008. Colloquium paper: resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. U. S. A. 105(Suppl 1):11512-11519. http://dx.doi.org/10.1073/pnas.0801925105.
2. Shade A, Peter H, Allison SD, Baho DL, Berga M, Burgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB, Matulich KL, Schmidt TM, Handelsman J. 2012. Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3:417. http://dx.doi.org/10.3389/fmicb.2012.00417.
3. Torsvik V, Goksoyr J, Daae FL. 1990. High diversity in DNA of soil bacteria. Appl. Environ. Microbiol. 56:782-787.
4. Whitman WB, Coleman DC, Wiebe WJ. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U. S. A. 95:6578-6583. http://dx.doi.org/10.1073/pnas.95.12.6578.
5. Curtis TP, Sloan WT, Scannell JW. 2002. Estimating prokaryotic diversity and its limits. Proc. Natl. Acad. Sci. U. S. A. 99:10494-10499. http://dx.doi.org/10.1073/pnas.142680199.
6. Handelsman J, Tiedje J, Alvarez-Cohen L, Ashburner M, Cann I, Delong E, Doolittle W, Fraser-Liggett C, Godzik A, Gordon J, Riley M, Schmidt T. 2007. The new science of metagenomics: revealing the secrets of our microbial planet. The National Academies Press, Washington, DC.
7. Konstantinidis KT, Tiedje JM. 2005. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. U. S. A. 102:2567-2572. http://dx.doi.org/10.1073/pnas.0409727102.
8. Nelson KE, Paulsen IT, Heidelberg JF, Fraser CM. 2000. Status of genome projects for nonpathogenic bacteria and archaea. Nat. Biotechnol. 18:1049-1054. http://dx.doi.org/10.1038/80235.
9. Bond-Lamberty B, Thomson A. 2010. Temperature-associated increases in the global soil respiration record. Nature 464:579-582. http://dx.doi.org/10.1038/nature08930.
10. Heimann M, Reichstein M. 2008. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289-292. http://dx.doi.org/10.1038/nature06591.
11. Deslippe JR, Hartmann M, Simard SW, Mohn WW. 2012. Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol. Ecol. 82:303-315. http://dx.doi.org/10.1111/j.1574-6941.2012.01350.x.
12. Deng Y, He Z, Xu M, Qin Y, Van Nostrand JD, Wu L, Roe BA, Wiley G, Hobbie SE, Reich PB, Zhou J. 2012. Elevated carbon dioxide alters the structure of soil microbial communities. Appl. Environ. Microbiol. 78: 2991-2995. http://dx.doi.org/10.1128/AEM.06924-11.
13. He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, Van Nostrand JD, Hobbie SE, Reich PB, Zhou J. 2010. Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol. Lett. 13:564-575. http://dx.doi.org/10.1111/j.1461-0248.2010.01453.x.
14. 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. Front. Microbiol. 2:94. http://dx.doi.org/10.3389/fmicb.2011.00094.
15. Dunbar J, Eichorst SA, Gallegos-Graves LV, Silva S, Xie G, Hengartner NW, Evans RD, Hungate BA, Jackson RB, Megonigal JP, Schadt CW, Vilgalys R, Zak DR, Kuske CR. 2012. Common bacterial responses in six ecosystems exposed to 10 years of elevated atmospheric carbon dioxide. Environ. Microbiol. 14:1145-1158. http://dx.doi.org/10.1111/j.1462-2920.2011.02695.x.
16. Sul WJ, Asuming-Brempong S, Wang Q, Tourlousse DM, Penton R, Deng Y, Rodrigues JLM, Adiku SGK, Jones JW, Zhou J, Cole JR, Tiedje JM. 2013. Tropical agricultural land management influences on soil microbial communities through its effect on soil organic carbon. Soil Biol. Biochem. 65:33-58. http://dx.doi.org/10.1016/j.soilbio.2013.05.007.
17. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R. 2012. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 6:1007-1017. http://dx.doi.org/10.1038/ismej.2011.159.
18. Konstantinidis KT, Tiedje JM. 2007. Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr. Opin. Microbiol. 10:504-509. http://dx.doi.org/10.1016/j.mib.2007.08.006.
19. Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ, Rubin EM, Jansson JK. 2011. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480:368-371. http://dx.doi.org/10.1038/nature10576.
20. Zhou J, Xue K, Xie J, Deng Y, Wu L, Cheng X, Fei S, Deng S, He Z, Van Nostrand JD, Luo Y. 2012. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Clim. Change 2:106-110. http://dx.doi.org/10.1038/nclimate1331.
21. Belay-Tedla A, Zhou XH, Su B, Wan SQ, Luo YQ. 2009. Labile, recalcitrant, and microbial carbon and nitrogen pools of a tallgrass prairie soil in the US Great Plains subjected to experimental warming and clipping. Soil Biol. Biochem. 41:110-116. http://dx.doi.org/10.1016/j.soilbio.2008.10.003.
22. Luo Y, Wan S, Hui D, Wallace LL. 2001. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622-625. http://dx.doi.org/10.1038/35098065.
23. Luo Y, White L, Hui D. 2004. Comment on "Impacts of fine root turnover on forest NPP and soil C sequestration potential." Science 304:1745 http://dx.doi.org/10.1126/science.1098080.
24. Sherry RA, Zhou X, Gu S, Arnone JA, III, Schimel DS, Verburg PS, Wallace LL, Luo Y. 2007. Divergence of reproductive phenology under climate warming. Proc. Natl. Acad. Sci. U. S. A. 104:198-202. http://dx.doi.org/10.1073/pnas.0605642104.
25. Zhou X, Wan SQ, Luo YQ. 2007. Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem. Glob. Chang. Biol. 13:761-775. http://dx.doi.org/10.1111/j.1365-2486.2007.01333.x.
26. Zhou J, Bruns MA, Tiedje JM. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.
27. Oh S, Tandukar M, Pavlostathis SG, Chain PSG, Konstantinidis KT. 2013. Microbial community adaptation to quaternary ammonium biocides as revealed by metagenomics. Environ. Microbiol. 15:2850-2864. http://dx.doi.org/10.1111/1462-2920.12154.
28. Luo C, Tsementzi D, Kyrpides NC, Konstantinidis KT. 2012. Individual genome assembly from complex community short-read metagenomic datasets. ISME J. 6:898-901. http://dx.doi.org/10.1038/ismej.2011.147.
29. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821-829. http://dx.doi.org/10.1101/gr.074492.107.
30. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20:265-272. http://dx.doi.org/10.1101/gr.097261.109.
31. Zhu W, Lomsadze A, Borodovsky M. 2010. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38:e132. http://dx.doi.org/10.1093/nar/gkq275.
32. Rho M, Tang H, Ye Y. 2010. FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res. 38:e191. http://dx.doi.org/10.1093/nar/gkq747.
33. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch GD, Rodionov DA, Ruckert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y, Zagnitko O, Vonstein V. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33:5691-5702. http://dx.doi.org/10.1093/nar/gki866.
34. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res. 12:656-664. http://dx.doi.org/10.1101/gr.229202.
35. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA. 2008. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. http://dx.doi.org/10.1186/1471-2105-9-386.
36. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069-5072. http://dx.doi.org/10.1128/AEM.03006-05.
37. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
38. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41: D590-D596. http://dx.doi.org/10.1093/nar/gks1219.
39. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145. http://dx.doi.org/10.1093/nar/gkn879.
40. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106. http://dx.doi.org/10.1186/gb-2010-11-10-r106.
41. Rodriguez-R LM, Konstantinidis KT. 5 November 2013. Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets. Bioinformatics. http://dx.doi.org/10.1093/bioinformatics/btt584.
42. Konstantinidis KT, Braff J, Karl DM, DeLong EF. 2009. Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at station ALOHA in the North Pacific subtropical gyre. Appl. Environ. Microbiol. 75:5345-5355. http://dx.doi.org/10.1128/AEM.00473-09.
43. Oh S, Caro-Quintero A, Tsementzi D, DeLeon-Rodriguez N, Luo C, Poretsky R, Konstantinidis KT. 2011. Metagenomic insights into the evolution, function, and complexity of the planktonic microbial community of Lake Lanier, a temperate freshwater ecosystem. Appl. Environ. Microbiol. 77:6000-6011. http://dx.doi.org/10.1128/AEM.00107-11.
44. 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. Proc. Natl. Acad. Sci. U. S. A. 109:21390-21395. http://dx.doi.org/10.1073/pnas.1215210110.
45. Cole J, Konstantinidis KT, Farris RJ, Tiedje JM. 2010. Microbial diversity and phylogeny: extending from rRNAs to genomes, p 1-20. In Liu W-T, Jansson J (ed), Environmental molecular biology. Horizon Scientific Press, Norwich, United Kingdom.
46. Caro-Quintero A, Konstantinidis KT. 2012. Bacterial species may exist, metagenomics reveal. Environ. Microbiol. 14:347-355. http://dx.doi.org/10.1111/j.1462-2920.2011.02668.x.
47. Lozupone C, Hamady M, Knight R. 2006. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371. http://dx.doi.org/10.1186/1471-2105-7-371.
48. Nakashima H, Fukuchi S, Nishikawa K. 2003. Compositional changes in RNA, DNA and proteins for bacterial adaptation to higher and lower temperatures. J. Biochem. 133:507-513. http://dx.doi.org/10.1093/jb/mvg067.
49. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW. 2003. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042-1047. http://dx.doi.org/10.1038/nature01947.
50. Turnbaugh PJ, Gordon JI. 2008. An invitation to the marriage of metagenomics and metabolomics. Cell 134:708-713. http://dx.doi.org/10.1016/j.cell.2008.08.025.
51. Hettich RL, Pan C, Chourey K, Giannone RJ. 2013. Metaproteomics: harnessing the power of high performance mass spectrometry to identify the suite of proteins that control metabolic activities in microbial communities. Anal. Chem. 85:4203-4214. http://dx.doi.org/10.1021/ac303053e.
52. Barberán A, Bates ST, Casamayor EO, Fierer N. 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 6:343-351. http://dx.doi.org/10.1038/ismej.2011.119.
53. Philippot L, Andersson SGE, Battin TJ, Prosser JI, Schimel JP, Whitman WB, Hallin S. 2010. The ecological coherence of high bacterial taxonomic ranks. Nat. Rev. Microbiol. 8:523-529. http://dx.doi.org/10.1038/nrmicro2367.
54. Konstantinidis KT, DeLong EF. 2008. Genomic patterns of recombination, clonal divergence and environment in marine microbial populations. ISME J. 2:1052-1065. http://dx.doi.org/10.1038/ismej.2008.62.
55. Lipson DA, Schmidt SK. 2004. Seasonal changes in an alpine soil bacterial community in the Colorado Rocky Mountains. Appl. Environ. Microbiol. 70:2867-2879. http://dx.doi.org/10.1128/AEM.70.5.2867-2879.2004.