Successional trajectories of rhizosphere bacterial communities over consecutive seasons

mBio

Volumn 6, Issue 4, 2015, Pages

  Shi, Shengjing ^a,b   Nuccio, Erin ^a,c   Herman, Donald J ^a,d   Rijkers, Ruud ^a   Estera, Katerina ^a   Li, Jiabao ^b   Da Rocha, Ulisses Nunes ^d   He, Zhili ^b   Pett Ridge, Jennifer ^c   Brodie, Eoin L ^a,d   Zhou, Jizhong ^b,d,e   Firestone, Mary ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; BACTERIAL DNA; RIBOSOME DNA;

ACIDOBACTERIA; ACTINOBACTERIA; ALPHAPROTEOBACTERIA; ARTICLE; AVENA FATUA; BACTEROIDETES; BETAPROTEOBACTERIA; COMMUNITY SUCCESSION; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; FIRMICUTES; GENETIC CONSERVATION; GROWING SEASON; HIGH THROUGHPUT SEQUENCING; MICROBIAL COMMUNITY; NONHUMAN; PHYLOGENY; PLANT GROWTH; PLANT ROOT; POPULATION ABUNDANCE; PRIORITY JOURNAL; REPRODUCIBILITY; RHIZOSPHERE BACTERIUM; SOIL MICROFLORA; SPECIES RICHNESS; TAXONOMY; AVENA; BIOTA; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; MICROBIOLOGY; RHIZOSPHERE; SEASON;

AVENA; BIOTA; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PHYLOGENY; PLANT ROOTS; RHIZOSPHERE; RNA, RIBOSOMAL, 16S; SEASONS; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

EID: 84940869067     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00746-15     Document Type: Article

References (59)

1. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. http://dx.doi.org/10.1146/annurev.arplant.57.032905.105159.
2. Shi S, Richardson AE, O’Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone MK, Condron LM. 2011. Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol Ecol 77: 600–610. http://dx.doi.org/10.1111/j.1574-6941.2011.01150.x.
3. Hinsinger P, Bengough AG, Vetterlein D, Young IM. 2009. Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321: 117–152. http://dx.doi.org/10.1007/s11104-008-9885-9.
4. da Rocha UN, Van Overbeek L, Van Elsas JD. 2009. Exploration of hitherto-uncultured bacteria from the rhizosphere. FEMS Microbiol Ecol 69:313–328. http://dx.doi.org/10.1111/j.1574-6941.2009.00702.x.
5. Mendes R, Garbeva P, Raaijmakers JM. 2013. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. http://dx.doi.org/10.1111/1574-6976.12028.
6. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, Piceno YM, DeSantis TZ, Andersen GL, Bakker PA, Raaijmakers JM. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100. http://dx.doi.org/10.1126/science.1203980.
7. Carney KM, Hungate BA, Drake BG, Megonigal JP. 2007. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci U S A 104:4990–4995. http://dx.doi.org/10.1073/pnas.0610045104.
8. Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13. http://dx.doi.org/10.1111/j.1574-6941.2009.00654.x.
9. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G. 2001. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67: 4742–4751. http://dx.doi.org/10.1128/AEM.67.10.4742-4751.2001.
10. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. 2013. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. http://dx.doi.org/10.1038/nrmicro3109.
11. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108(Suppl 1):4516–4522. http://dx.doi.org/10.1073/pnas.1000080107.
12. 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.
13. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110:6548–6553. http://dx.doi.org/10.1073/pnas.1302837110.
14. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. http://dx.doi.org/10.1038/nature11237.
15. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95. http://dx.doi.org/10.1038/nature11336.
16. Chaparro JM, Badri DV, Vivanco JM. 2014. Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. http://dx.doi.org/10.1038/ismej.2013.196.
17. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ. 2002. Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. http://dx.doi.org/10.1146/annurev.ecolsys.33.010802.150448.
18. DeAngelis KM, Brodie EL, DeSantis TZ, Andersen GL, Lindow SE, Firestone MK. 2009. Selective progressive response of soil microbial community to wild oat roots. ISME J 3:168–178. http://dx.doi.org/10.1038/ismej.2008.103.
19. Schreiter S, Ding G-C, Heuer H, Neumann G, Sandmann M, Grosch R, Kropf S, Smalla K. 2014. Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front Microbiol 5:144. http://dx.doi.org/10.3389/fmicb.2014.00144.
20. Li X, Rui J, Mao Y, Yannarell A, Mackie R. 2014. Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil B i o l Biochem 6 8:392–401. http://dx.doi.org/10.1016j.soilbio.2013.10.017.
21. Singh G, Mukerji KG. 2006. Root exudates as determinant of rhizospheric microbial biodiversity, p 39–54. In Mukerji KG, Manoharachary C, Singh J (ed), Microbial activity in the rhizosphere. Springer, Berlin, Germany.
22. Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM. 2013. Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS One 8:e55731. http://dx.doi.org/10.1371/journal.pone.0055731.
23. Torsvik V, Øvreås L, Thingstad TF. 2002. Prokaryotic diversity— magnitude, dynamics, and controlling factors. Science 296:1064–1066. http://dx.doi.org/10.1126/science.1071698.
24. Fierer N, Lennon JT. 2011. The generation and maintenance of diversity in microbial communities. Am J Bot 98:439–448. http://dx.doi.org/10.3732/ajb.1000498.
25. Smalla K, Van Elsas JD. 2010. The soil environment, p 111–130. In Liu W-T, Jasson JK (ed), Environmental molecular microbiology. Caister Academic Press, Poole, Dorset, United Kingdom.
26. Leibold MA, McPeek MA. 2006. Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410. http://dx.doi.org/10.1890/0012-9658(2006)87[1399:COTNAN]2.0.CO;2.
27. Costa R, Götz M, Mrotzek N, Lottmann J, Berg G, Smalla K. 2006. Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249. http://dx.doi.org/10.1111/j.1574-6941.2005.00026.x.
28. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PG, van Veen JA. 2002. Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 81:509–520. http://dx.doi.org/10.1023/A:1020565523615.
29. Uroz S, Buée M, Murat C, Frey-Klett P, Martin F. 2010. Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2:281–288. http://dx.doi.org/10.1111/j.1758-2229.2009.00117.x.
30. Hawkes CV, DeAngelis KM, Firestone MK. 2007. Root interactions with soil microbial communities and processes, p 1–31. In Cardon ZG, Whitbeck JL (ed), The rhizosphere: an ecological perspective. Elsevier Inc, New York, NY.
31. Fierer N, Bradford MA, Jackson RB. 2007. Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. http://dx.doi.org/10.1890/05-1839.
32. 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.
33. Vandenkoornhuyse P, Mahé S, Ineson P, Staddon P, Ostle N, Cliquet J-B, Francez A-J, Fitter AH, Young JP. 2007. Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc Natl Acad Sci U S A 104:16970–16975. http://dx.doi.org/10.1073/pnas.0705902104.
34. Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, AchouakW. 2008. Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230. http://dx.doi.org/10.1038/ismej.2008.80.
35. Shi S, Condron L, Larsen S, Richardson AE, Jones E, Jiao J, O’Callaghan M, Stewart A. 2011. In situ sampling of low molecular weight organic anions from rhizosphere of Radiata pine (Pinus radiata) grown in a rhizotron system. Environ Exp Bot 70:131–142. http://dx.doi.org/10.1016/j.envexpbot.2010.08.010.
36. Shi S, O’Callaghan M, Jones EE, Richardson AE, Walter C, Stewart A, Condron L. 2012. Investigation of organic anions in tree root exudates and rhizosphere microbial communities using in situ and destructive sampling techniques. Plant Soil 359:149–163. http://dx.doi.org/10.1007/s11104-012-1198-3.
37. 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. Appl Environ Microbiol 75:5111–5120. http://dx.doi.org/10.1128/AEM.00335-09.
38. Kielak A, Pijl AS, van Veen JA, Kowalchuk GA. 2009. Phylogenetic diversity of acidobacteria in a former agricultural soil. ISME J 3:378–382. http://dx.doi.org/10.1038/ismej.2008.113.
39. Nuccio E. 2013. Deconstructing the soil microbiome: elucidating the influence of roots and arbuscular mycorrhizae on soil microbial communities. Ph.D. thesis. University of California, Berkeley, California.
40. Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR. 2012. Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93:1867–1879. http://dx.doi.org/10.1890/11-1745.1.
41. Placella SA, Brodie EL, Firestone MK. 2012. Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc Natl Acad Sci U S A 109:10931–10936. http://dx.doi.org/10.1073/pnas.1204306109.
42. Philippot L, Andersson SG, 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.
43. Barnard RL, Osborne CA, Firestone MK. 2013. Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241. http://dx.doi.org/10.1038/ismej.2013.104.
44. Hawkes CV, Wren IF, Herman DJ, Firestone MK. 2005. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985. http://dx.doi.org/10.1111/j.1461-0248.2005.00802.x.
45. Hawkes CV, Belnap J, D’Antonio C, Firestone MK. 2006. Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant Soil 281:369–380. http://dx.doi.org/10.1007/s11104-005-4826-3.
46. Fierer N, Jackson JA, Vilgalys R, Jackson RB. 2005. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120. http://dx.doi.org/10.1128/AEM.71.7.4117-4120.2005.
47. Kong Y. 2011. Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics 98: 152–153. http://dx.doi.org/10.1016/j.ygeno.2011.05.009.
48. Magocˇ T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. http://dx.doi.org/10.1093/bioinformatics/btr507.
49. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200. http://dx.doi.org/10.1093/bioinformatics/btr381.
50. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
51. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. http://dx.doi.org/10.1128/AEM.00062-07.
52. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. http://dx.doi.org/10.1371/journal.pone.0009490.
53. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. http://dx.doi.org/10.1093/bioinformatics/btq166.
54. Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK. 2013. An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15:1870–1881. http://dx.doi.org/10.1111/1462-2920.12081.
55. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. http://dx.doi.org/10.1093/bioinformatics/btg412.
56. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. http://dx.doi.org/10.1046/j.1442-9993.2001.01070.x.
57. Anderson MJ, Ellingsen KE, McArdle BH. 2006. Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. http://dx.doi.org/10.1111/j.1461-0248.2006.00926.x.
58. Anderson MJ. 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. http://dx.doi.org/10.1111/j.1541-0420.2005.00440.x.
59. Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos PM, Stevens HH, Wagner H. 2013. vegan: community ecology package. Package version 20-10. R Project, Vienna, Austria.