Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil

Soil Biology and Biochemistry

Volumn 97, Issue , 2016, Pages 188-198

  Banerjee, Samiran ^a   Kirkby, Clive A ^a   Schmutter, Dione ^a   Bissett, Andrew ^a   Kirkegaard, John A ^a   Richardson, Alan E ^a  

^a Clunies Ross Street   (Australia)

Author keywords

Co occurrence; Decomposition; Keystone taxa; Network analysis; Organic matter

Indexed keywords

AGRICULTURAL WASTES; AGRICULTURE; ARCHES; BACTERIA; BIOGEOCHEMISTRY; BIOLOGICAL MATERIALS; BIOLOGY; BIOMASS; CARBON; DECOMPOSITION; ELECTRIC NETWORK ANALYSIS; NUTRIENTS; ORGANIC COMPOUNDS; REDUNDANCY; RNA;

BACTERIAL COMMUNITY; CO-OCCURRENCE; CO-OCCURRENCE PATTERN; FUNCTIONAL REDUNDANCY; KEYSTONE TAXA; MICROBIAL DECOMPOSITION; MICROCOSM EXPERIMENTS; ORGANIC MATTER DECOMPOSITION;

FUNGI;

ABUNDANCE; AGRICULTURAL SOIL; BIOMASS; CARBON SEQUESTRATION; CROP RESIDUE; DECOMPOSITION; FUNGUS; GENETIC ANALYSIS; KEYSTONE SPECIES; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROCOSM; NETWORK ANALYSIS; NUTRIENT DYNAMICS; ORGANIC MATTER; SPECIES DIVERSITY; SPECIES EVENNESS; SPECIES RICHNESS;

ACIDOBACTERIA; BACTERIA (MICROORGANISMS); CEPHALOTHECA; CHAETOMIUM; FRATEURIA; FUNGI; FUSARIUM; GEMMATIMONAS;

EID: 84962013770     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2016.03.017     Document Type: Article

References (60)

1. Allison S.D., Martiny J.B.H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(Suppl.):11512-11519. 10.1073/pnas.0801925105.
2. Allison S.D., Hanson C.a., Treseder K.K. Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biol. Biochem. 2007, 39:1878-1887. 10.1016/j.soilbio.2007.02.001.
3. Allison S.D., Czimczik C.I., Treseder K.K. Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob. Chang. Biol. 2008, 14:1156-1168. 10.1111/j.1365-2486.2008.01549.x.
4. Allison S.D., Wallenstein M.D., Bradford M.a. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 2010, 3:336-340. 10.1038/ngeo846.
5. Banerjee S., Baah-Acheamfour M., Carlyle C.N., Bissett A., Richardson A.E., Siddique T., Bork E., Chang S. Determinants of bacterial communities in Canadian agroforestry systems. Environ. Microbiol. 2015, (Epub ahead of print). 10.1111/1462-2920.12986.
6. Barberán A., Bates S.T., Casamayor E.O., Fierer N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 2012, 6:343-351. 10.1038/ismej.2011.119.
7. Bardgett R.D., McAlister E. The measurement of soil fungal:bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biol. Fertil. Soils 1999, 29:282-290. 10.1007/s003740050554.
8. Bardgett R.D., Hobbs P.J., Frostegård Å. Changes in soil fungal:bacterial biomass ratios following reductions in the intensity of management of an upland grassland. Biol. Fertil. Soils 1996, 22:261-264. 10.1007/s003740050108.
9. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 1995, 57:289-300.
10. Bissett A., Brown M.V., Siciliano S.D., Thrall P.H. Microbial community responses to anthropogenically induced environmental change: towards a systems approach. Ecol. Lett. 2013, 16:128-139. 10.1111/ele.12109.
11. Blagodatskaya Ye{cyrillic}., Kuzyakov Y. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol. Fertil. Soils 2008, 45:115-131. 10.1007/s00374-008-0334-y.
12. Burke C., Steinberg P., Rusch D., Kjelleberg S., Thomas T. Bacterial community assembly based on functional genes rather than species. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14288-14293. 10.1073/pnas.1101591108.
13. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., Mcdonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. QIIME allows analysis of high- throughput community sequencing data. Nat. Methods 2010, 7:335-336. 10.1038/nmeth0510-335.
14. Chèneby D., Philippot L., Hartmann a, Hénault C., Germon J. 16S rDNA analysis for characterization of denitrifying bacteria isolated from three agricultural soils. FEMS Microbiol. Ecol. 2000, 34:121-128. 10.1111/j.1574-6941.2000.tb00761.x.
15. Clarke K.R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 1993, 18:117-143.
16. Cleveland C.C., Nemergut D.R., Schmidt S.K., Townsend A.R. Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 2007, 82:229-240. 10.1007/s10533-006-9065-z.
17. Dowd S.E., et al. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 2008, 8:125. 10.1186/1471-2180-8-125.
18. Dungait, Hopkins D.W., Gregory A.S., Whitmore A.P. Soil organic matter turnover is governed by accessibility not recalcitrance. Glob. Chang. Biol. 2012, 18:1781-1796. 10.1111/j.1365-2486.2012.02665.x.
19. Edgar R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461. 10.1093/bioinformatics/btq461.
20. Ferrari B.C., Bissett A., Snape I., van Dorst J., Palmer A.S., Ji M., Siciliano S.D., Stark J.S., Winsley T., Brown M.V. Geological connectivity drives microbial community structure and connectivity in polar, terrestrial ecosystems. Environ. Microbiol. 2015, (Epub ahead of print). 10.1111/1462-2920.13034.
21. Fierer N., Bradford M.A., Jackson R.A. Toward an ecological classification of soil bacteria. Ecology 2007, 88:1354-1364.
22. Fontaine S., Mariotti A., Abbadie L. The priming effect of organic matter: a question of microbial competition?. Soil Biol. Biochem. 2003, 35:837-843. 10.1016/S0038-0717(03)00123-8.
23. Fuhrman J.A. Microbial community structure and its functional implications. Nature 2009, 459:193-199. 10.1038/nature08058.
24. Gardes M., Bruns T.D. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993, 2:113-118.
25. Gilbert J.a, Steele J.a, Caporaso J.G., Steinbruck L., Reeder J., Temperton B., Huse S., McHardy a C., Knight R., Joint I., Somerfield P., Fuhrman J.a, Field D. Defining seasonal marine microbial community dynamics. ISME J. 2012, 6:298-308. 10.1038/ismej.2011.107.
26. Goldfarb K.C., Karaoz U., Hanson C.a, Santee C.a, Bradford M.a, Treseder K.K., Wallenstein M.D., Brodie E.L. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front. Microbiol. 2011, 2:94. 10.3389/fmicb.2011.00094.
27. Grandy a.S., Neff J.C. Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci. Total Environ. 2008, 404:297-307. 10.1016/j.scitotenv.2007.11.013.
28. Harreither W., Sygmund C., Augustin M., Narciso M., Rabinovich M.L., Gorton L., Haltrich D., Ludwig R. Catalytic properties and classification of cellobiose dehydrogenases from ascomycetes. Appl. Environ. Microbiol. 2011, 77:1804-1815. 10.1128/AEM.02052-10.
29. Isbell R. The Australian soil classification. Australian Soil and Land Survey Handbook 2002, Commonwealth Scientific and Industrial Research Organisation, Collingwood, Victoria, Australia, Series 4.
30. Kirkby C.a., Kirkegaard J.a., Richardson a.E., Wade L.J., Blanchard C., Batten G. Stable soil organic matter: a comparison of C: N:P: S ratios in Australian and other world soils. Geoderma 2011, 163:197-208. 10.1016/j.geoderma.2011.04.010.
31. Kirkby C.a., Richardson a.E., Wade L.J., Blanchard C., Batten G., Kirkegaard J.a. Carbon-nutrient stoichiometry to increase soil carbon sequestration. Soil Biol. Biochem. 2013, 60:77-86. 10.1016/j.soilbio.2013.01.011.
32. Kirkby C.a., Richardson a.E., Wade L.J., Blanchard C., Batten G., Kirkegaard J.a., Passioura J.B. Nutrient availability limits carbon sequestration in arable soils. Soil Biol. Biochem. 2014, 68:402-409. 10.1016/j.soilbio.2013.09.032.
33. Kirkegaard J.A., Angus J.F., Gardner P.A., Muller W. Reduced growth and yield of wheat with conservation cropping.1. Field studies in the 1St year of the cropping phase. Aust. J. Agric. Res. 1994, 45:511-528.
34. Kõljalg U., Larsson K.-H., Abarenkov K., Nilsson R.H., Alexander I.J., Eberhardt U., Erland S., Høiland K., Kjøller R., Larsson E., Pennanen T., Sen R., Taylor A.F.S., Tedersoo L., Vrålstad T., Ursing B.M. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol. 2005, 166:1063-1068. 10.1111/j.1469-8137.2005.01376.x.
35. Lal R. Soil carbon sequestration impacts on global climate change and food security. Science 2004, 304:1623-1627. 80-.
36. Li R., Khafipour E., Krause D.O., Entz M.H., de Kievit T.R., Fernando W.G.D. Pyrosequencing reveals the influence of organic and conventional farming systems on bacterial communities. PLoS One 2012, 7. 10.1371/journal.pone.0051897.
37. Liang C., Balser T.C. Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat. Rev. Microbiol. 2011, 9:75. 10.1038/nrmicro2386-c1.
38. Lozupone C., Knight R. UniFrac[U+202F]: a new phylogenetic method for comparing microbial communities 2005, 71. 10.1128/AEM.71.12.8228.
39. Mau R.L., Liu C.M., Aziz M., Schwartz E., Dijkstra P., Marks J.C., Price L.B., Keim P., Hungate B.a Linking soil bacterial biodiversity and soil carbon stability. ISME J. 2014, 9:1477-1480. 10.1038/ismej.2014.205.
40. Nilsson R.H., Kristiansson E., Ryberg M., Hallenberg N., Larsson K.H. Intraspecific ITS variability in the Kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol. Bioinforma. 2008, 2008:193-201. 10.4137/EBO.S653.
41. Ovreås L., Forney L., Daae F.L. Distribution of bacterioplankton in Meromictic Lake Sælenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA 1997, 63:3367-3373.
42. Prosser J.I., Bohannan B.J.M., Curtis T.P., Ellis R.J., Firestone M.K., Freckleton R.P., Green J.L., Green L.E., Killham K., Lennon J.J., Osborn a M., Solan M., van der Gast C.J., Young J.P.W. The role of ecological theory in microbial ecology. Nat. Rev. Microbiol. 2007, 5:384-392. 10.1038/nrmicro1643.
43. Pruesse E., Quast C., Knittel K., Fuchs B.M., Ludwig W., Peplies J., Glöckner F.O. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35:7188-7196. 10.1093/nar/gkm864.
44. Rawat S.R., Männistö M.K., Bromberg Y., Häggblom M.M. Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils. FEMS Microbiol. Ecol. 2012, 82:341-355. 10.1111/j.1574-6941.2012.01381.x.
45. Reshef D.N., Reshef Y.a, Finucane H.K., Grossman S.R., McVean G., Turnbaugh P.J., Lander E.S., Mitzenmacher M., Sabeti P.C. Detecting novel associations in large data sets. Science 2011, 334:1518-1524. 10.1126/science.1205438.
46. Richardson A.E., Kirkby C.A., Banerjee S., Kirkegaard J.A. The inorganic nutrient cost of building soil carbon. Carbon Manag. 2014, 5:265-268. 10.1080/17583004.2014.923226.
47. Schimel J.P., Schaeffer S.M. Microbial control over carbon cycling in soil. Front. Microbiol. 2012, 3:348. 10.3389/fmicb.2012.00348.
48. Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.a, Oakley B.B., Parks D.H., Robinson C.J., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J., Weber C.F. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75:7537-7541. 10.1128/AEM.01541-09.
49. Schmidt M.W.I., Torn M.S., Abiven S., Dittmar T., Guggenberger G., Janssens I.a, Kleber M., Kögel-Knabner I., Lehmann J., Manning D.a C., Nannipieri P., Rasse D.P., Weiner S., Trumbore S.E. Persistence of soil organic matter as an ecosystem property. Nature 2011, 478:49-56. 10.1038/nature10386.
50. Scow K.M. Ecology in agriculture. Ecology in Agriculture 1997, 367-413. Academic Press, San Diego, CA. L.E. Jackson (Ed.).
51. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape[U+202F]: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 2498-2504. 10.1101/gr.1239303.metabolite.
52. Six J., Frey S.D., Thiet R.K., Batten K.M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 2006, 70:555. 10.2136/sssaj2004.0347.
53. Sollins P., Homann P., Caldwell B.a Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 1996, 74:65-105. 10.1016/S0016-7061(96)00036-5.
54. Trivedi P., Anderson I.C., Singh B.K. Microbial modulators of soil carbon storage[U+202F]: integrating genomic and metabolic knowledge for global prediction. Trends Microbiol. 2013, 21:641-651. 10.1016/j.tim.2013.09.005.
55. Tveit A.T., Urich T., Svenning M.M. Metatranscriptomic analysis of arctic peat soil microbiota. Appl. Environ. Microbiol. 2014, 80:5761-5772. 10.1128/AEM.01030-14.
56. van der Heijden M.G.a, Bardgett R.D., van Straalen N.M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 2008, 11:296-310. 10.1111/j.1461-0248.2007.01139.x.
57. Vick-Majors T.J., Priscu J.C., Amaral-Zettler L.a Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes. ISME J. 2014, 8:778-789. 10.1038/ismej.2013.190.
58. Walse C., Berg B., Sverdrup H. Review and synthesis of experimental data on organic matter decomposition with respect to the effect of temperature, moisture, and acidity. Environ. Rev. 2011, 40.
59. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73:5261-5267. 10.1128/AEM.00062-07.
60. Wieder W.R., Bonan G.B., Allison S.D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Chang. 2013, 3:909-912. 10.1038/nclimate1951.