Disentangling the Influence of Earthworms in Sugarcane Rhizosphere

Overview

Journal Sci Rep

Specialty Science

Date 2016 Dec 16

PMID 27976685

Citations 9

Authors

Lucas P P Braga

Caio A Yoshiura

Clovis D Borges

Marcus A Horn

George G Brown

Harold L Drake

Siu M Tsai

Affiliations

Soon will be listed here.

Abstract

For the last 150 years many studies have shown the importance of earthworms for plant growth, but the exact mechanisms involved in the process are still poorly understood. Many important functions required for plant growth can be performed by soil microbes in the rhizosphere. To investigate earthworm influence on the rhizosphere microbial community, we performed a macrocosm experiment with and without Pontoscolex corethrurus (EW+ and EW-, respectively) and followed various soil and rhizosphere processes for 217 days with sugarcane. In EW+ treatments, NO concentrations belowground (15 cm depth) and relative abundances of nitrous oxide genes (nosZ) were higher in bulk soil and rhizosphere, suggesting that soil microbes were able to consume earthworm-induced NO. Shotgun sequencing (total DNA) revealed that around 70 microbial functions in bulk soil and rhizosphere differed between EW+ and EW- treatments. Overall, genes indicative of biosynthetic pathways and cell proliferation processes were enriched in EW+ treatments, suggesting a positive influence of worms. In EW+ rhizosphere, functions associated with plant-microbe symbiosis were enriched relative to EW- rhizosphere. Ecological networks inferred from the datasets revealed decreased niche diversification and increased keystone functions as an earthworm-derived effect. Plant biomass was improved in EW+ and worm population proliferated.

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References

Henry S, Bru D, Stres B, Hallet S, Philippot L . Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol. 2006; 72(8):5181-9. PMC: 1538733. DOI: 10.1128/AEM.00231-06. View

Bruto M, Prigent-Combaret C, Muller D, Moenne-Loccoz Y . Analysis of genes contributing to plant-beneficial functions in Plant Growth-Promoting Rhizobacteria and related Proteobacteria. Sci Rep. 2014; 4:6261. PMC: 4151105. DOI: 10.1038/srep06261. View

Henry S, Texier S, Hallet S, Bru D, Dambreville C, Cheneby D . Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environ Microbiol. 2008; 10(11):3082-92. DOI: 10.1111/j.1462-2920.2008.01599.x. View

Horn M, Ihssen J, Matthies C, Schramm A, Acker G, Drake H . Dechloromonas denitrificans sp. nov., Flavobacterium denitrificans sp. nov., Paenibacillus anaericanus sp. nov. and Paenibacillus terrae strain MH72, N2O-producing bacteria isolated from the gut of the earthworm Aporrectodea caliginosa. Int J Syst Evol Microbiol. 2005; 55(Pt 3):1255-1265. DOI: 10.1099/ijs.0.63484-0. View

Liu Y, Zaprasis A, Liu S, Drake H, Horn M . The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders. ISME J. 2010; 5(3):473-85. PMC: 3105722. DOI: 10.1038/ismej.2010.140. View

Parks D, Tyson G, Hugenholtz P, Beiko R . STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014; 30(21):3123-4. PMC: 4609014. DOI: 10.1093/bioinformatics/btu494. View

Zhang J, Kobert K, Flouri T, Stamatakis A . PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2013; 30(5):614-20. PMC: 3933873. DOI: 10.1093/bioinformatics/btt593. View

Faust K, Raes J . Microbial interactions: from networks to models. Nat Rev Microbiol. 2012; 10(8):538-50. DOI: 10.1038/nrmicro2832. View

Mitchell A, Chang H, Daugherty L, Fraser M, Hunter S, Lopez R . The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 2014; 43(Database issue):D213-21. PMC: 4383996. DOI: 10.1093/nar/gku1243. View

10.

Schulz K, Hunger S, Brown G, Tsai S, Cerri C, Conrad R . Methanogenic food web in the gut contents of methane-emitting earthworm Eudrilus eugeniae from Brazil. ISME J. 2015; 9(8):1778-92. PMC: 4511933. DOI: 10.1038/ismej.2014.262. View

11.

Heuer H, Krsek M, Baker P, Smalla K, Wellington E . Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol. 1997; 63(8):3233-41. PMC: 168621. DOI: 10.1128/aem.63.8.3233-3241.1997. View

12.

Ihssen J, Horn M, Matthies C, Gossner A, Schramm A, Drake H . N2O-producing microorganisms in the gut of the earthworm Aporrectodea caliginosa are indicative of ingested soil bacteria. Appl Environ Microbiol. 2003; 69(3):1655-61. PMC: 150113. DOI: 10.1128/AEM.69.3.1655-1661.2003. View

13.

Jarchow S, Luck C, Gorg A, Skerra A . Identification of potential substrate proteins for the periplasmic Escherichia coli chaperone Skp. Proteomics. 2008; 8(23-24):4987-94. DOI: 10.1002/pmic.200800288. View

14.

Kuzyakov Y, Xu X . Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol. 2013; 198(3):656-669. DOI: 10.1111/nph.12235. View

15.

Estabrook E, Sengupta-Gopalan C . Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development. Plant Cell. 1991; 3(3):299-308. PMC: 160000. DOI: 10.1105/tpc.3.3.299. View

16.

Furlong M, Singleton D, Coleman D, Whitman W . Molecular and culture-based analyses of prokaryotic communities from an agricultural soil and the burrows and casts of the earthworm Lumbricus rubellus. Appl Environ Microbiol. 2002; 68(3):1265-79. PMC: 123750. DOI: 10.1128/AEM.68.3.1265-1279.2002. View

17.

Depkat-Jakob P, Brown G, Tsai S, Horn M, Drake H . Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa. FEMS Microbiol Ecol. 2012; 83(2):375-91. DOI: 10.1111/j.1574-6941.2012.01476.x. View

18.

Canellas L, Olivares F, Okorokova-Facanha A, Facanha A . Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol. 2002; 130(4):1951-7. PMC: 166705. DOI: 10.1104/pp.007088. View

19.

Dallinger A, Horn M . Agricultural soil and drilosphere as reservoirs of new and unusual assimilators of 2,4-dichlorophenol carbon. Environ Microbiol. 2013; 16(1):84-100. DOI: 10.1111/1462-2920.12209. View

20.

Ding W, Cai Y, Cai Z, Yagi K, Zheng X . Nitrous oxide emissions from an intensively cultivated maize-wheat rotation soil in the North China Plain. Sci Total Environ. 2007; 373(2-3):501-11. DOI: 10.1016/j.scitotenv.2006.12.026. View