Influence of Edaphic, Climatic, and Agronomic Factors on the Composition and Abundance of Nitrifying Microorganisms in the Rhizosphere of Commercial Olive Crops

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2015 May 8

PMID 25950678

Citations 24

Authors

Joan Caliz

Miguel Montes-Borrego

Xavier Triado-Margarit

Madis Metsis

Blanca B Landa

Emilio O Casamayor

Affiliations

Soon will be listed here.

Abstract

The microbial ecology of the nitrogen cycle in agricultural soils is an issue of major interest. We hypothesized a major effect by farm management systems (mineral versus organic fertilizers) and a minor influence of soil texture and plant variety on the composition and abundance of microbial nitrifiers. We explored changes in composition (16S rRNA gene) of ammonia-oxidizing archaea (AOA), bacteria (AOB), and nitrite-oxidizing bacteria (NOB), and in abundance of AOA and AOB (qPCR of amoA genes) in the rhizosphere of 96 olive orchards differing in climatic conditions, agricultural practices, soil properties, and olive variety. Majority of archaea were 1.1b thaumarchaeota (soil crenarchaeotic group, SCG) closely related to the AOA genus Nitrososphaera. Most AOB (97%) were identical to Nitrosospira tenuis and most NOB (76%) were closely related to Nitrospira sp. Common factors shaping nitrifiers assemblage composition were pH, soil texture, and olive variety. AOB abundance was positively correlated with altitude, pH, and clay content, whereas AOA abundances showed significant relationships with organic nitrogen content and exchangeable K. The abundances of AOA differed significantly among soil textures and olive varieties, and those of AOB among soil management systems and olive varieties. Overall, we observed minor effects by orchard management system, soil cover crop practices, plantation age, or soil organic matter content, and major influence of soil texture, pH, and olive tree variety.

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References

Pruesse E, Peplies J, Glockner F . SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012; 28(14):1823-9. PMC: 3389763. DOI: 10.1093/bioinformatics/bts252. View

Di H, Cameron K, Shen J, Winefield C, OCallaghan M, Bowatte S . Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol. 2010; 72(3):386-94. DOI: 10.1111/j.1574-6941.2010.00861.x. View

Vitousek P, Menge D, Reed S, Cleveland C . Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc Lond B Biol Sci. 2013; 368(1621):20130119. PMC: 3682739. DOI: 10.1098/rstb.2013.0119. View

Zohary D, Spiegel-Roy P . Beginnings of fruit growing in the old world. Science. 1975; 187(4174):319-27. DOI: 10.1126/science.187.4174.319. View

Edgar R . UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013; 10(10):996-8. DOI: 10.1038/nmeth.2604. View

Luna G, Stumm K, Pusceddu A, Danovaro R . Archaeal diversity in deep-sea sediments estimated by means of different terminal-restriction fragment length polymorphisms (T-RFLP) protocols. Curr Microbiol. 2009; 59(3):356-61. DOI: 10.1007/s00284-009-9445-4. View

Bodirsky B, Popp A, Lotze-Campen H, Dietrich J, Rolinski S, Weindl I . Reactive nitrogen requirements to feed the world in 2050 and potential to mitigate nitrogen pollution. Nat Commun. 2014; 5:3858. DOI: 10.1038/ncomms4858. View

Glaser K, Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S . Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol. 2010; 74(3):575-91. DOI: 10.1111/j.1574-6941.2010.00970.x. View

Auguet J, Barberan A, Casamayor E . Global ecological patterns in uncultured Archaea. ISME J. 2009; 4(2):182-90. DOI: 10.1038/ismej.2009.109. View

10.

Palomares-Rius J, Castillo P, Montes-Borrego M, Navas-Cortes J, Landa B . Soil properties and olive cultivar determine the structure and diversity of plant-parasitic nematode communities infesting olive orchards soils in southern Spain. PLoS One. 2015; 10(1):e0116890. PMC: 4308072. DOI: 10.1371/journal.pone.0116890. View

11.

Ponti L, Gutierrez A, Ruti P, DellAquila A . Fine-scale ecological and economic assessment of climate change on olive in the Mediterranean Basin reveals winners and losers. Proc Natl Acad Sci U S A. 2014; 111(15):5598-603. PMC: 3992662. DOI: 10.1073/pnas.1314437111. View

12.

Rotthauwe J, Witzel K, Liesack W . The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol. 1997; 63(12):4704-12. PMC: 168793. DOI: 10.1128/aem.63.12.4704-4712.1997. View

13.

Landa B, Montes-Borrego M, Aranda S, Soriano M, Gomez J, Navas-Cortes J . Soil factors involved in the diversity and structure of soil bacterial communities in commercial organic olive orchards in Southern Spain. Environ Microbiol Rep. 2014; 6(2):196-207. DOI: 10.1111/1758-2229.12148. View

14.

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P . The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012; 41(Database issue):D590-6. PMC: 3531112. DOI: 10.1093/nar/gks1219. View

15.

Fowler D, Coyle M, Skiba U, Sutton M, Neil Cape J, Reis S . The global nitrogen cycle in the twenty-first century. Philos Trans R Soc Lond B Biol Sci. 2013; 368(1621):20130164. PMC: 3682748. DOI: 10.1098/rstb.2013.0164. View

16.

Verhamme D, Prosser J, Nicol G . Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 2011; 5(6):1067-71. PMC: 3131854. DOI: 10.1038/ismej.2010.191. View

17.

Martens-Habbena W, Berube P, Urakawa H, de la Torre J, Stahl D . Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature. 2009; 461(7266):976-9. DOI: 10.1038/nature08465. View

18.

Auguet J, Triado-Margarit X, Nomokonova N, Camarero L, Casamayor E . Vertical segregation and phylogenetic characterization of ammonia-oxidizing Archaea in a deep oligotrophic lake. ISME J. 2012; 6(9):1786-97. PMC: 3425235. DOI: 10.1038/ismej.2012.33. View

19.

Sliwinski M, Goodman R . Comparison of crenarchaeal consortia inhabiting the rhizosphere of diverse terrestrial plants with those in bulk soil in native environments. Appl Environ Microbiol. 2004; 70(3):1821-6. PMC: 368328. DOI: 10.1128/AEM.70.3.1821-1826.2004. View

20.

Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman F, Costello E . QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7(5):335-6. PMC: 3156573. DOI: 10.1038/nmeth.f.303. View