Assembly of Root-associated N2O-reducing Communities of Annual Crops is Governed by Selection for NosZ Clade I over Clade II

Overview

Journal FEMS Microbiol Ecol

Publisher Oxford University Press

Specialties Environmental Health
Microbiology

Date 2022 Aug 4

PMID 35927461

Authors

Daniel R H Graf

Christopher M Jones

Ming Zhao

Sara Hallin

Affiliations

Soon will be listed here.

Abstract

The rhizosphere is a hotspot for denitrification. The nitrous oxide (N2O) reductase among denitrifiers and nondenitrifying N2O reducers is the only known N2O sink in the biosphere. We hypothesized that the composition of root-associated N2O-reducing communities when establishing on annual crops depend on soil type and plant species, but that assembly processes are independent of these factors and differ between nosZ clades I and II. Using a pot experiment with barley and sunflower and two soils, we analyzed the abundance, composition, and diversity of soil and root-associated N2O reducing communities by qPCR and amplicon sequencing of nosZ. Clade I was more abundant on roots compared to soil, while clade II showed the opposite. In barley, this pattern coincided with N2O availability, determined as potential N2O production rates, but for sunflower no N2O production was detected in the root compartment. Root and soil nosZ communities differed in composition and phylogeny-based community analyses indicated that assembly of root-associated N2O reducers was driven by the interaction between plant and soil type, with inferred competition being more influential than habitat selection. Selection between clades I and II in the root/soil interface is suggested, which may have functional consequences since most clade I microorganisms can produce N2O.

References

Caruso T, Chan Y, Lacap D, Lau M, McKay C, Pointing S . Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J. 2011; 5(9):1406-13. PMC: 3160679. DOI: 10.1038/ismej.2011.21. View

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

Bulgarelli D, Garrido-Oter R, Munch P, Weiman A, Droge J, Pan Y . Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe. 2015; 17(3):392-403. PMC: 4362959. DOI: 10.1016/j.chom.2015.01.011. View

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

Conrad R . Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev. 1996; 60(4):609-40. PMC: 239458. DOI: 10.1128/mr.60.4.609-640.1996. View

Hallin S, Philippot L, Loffler F, Sanford R, Jones C . Genomics and Ecology of Novel NO-Reducing Microorganisms. Trends Microbiol. 2017; 26(1):43-55. DOI: 10.1016/j.tim.2017.07.003. View

Mendes L, Kuramae E, Navarrete A, van Veen J, Tsai S . Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J. 2014; 8(8):1577-87. PMC: 4817605. DOI: 10.1038/ismej.2014.17. View

Tkacz A, Cheema J, Chandra G, Grant A, Poole P . Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition. ISME J. 2015; 9(11):2349-59. PMC: 4611498. DOI: 10.1038/ismej.2015.41. View

Fish J, Chai B, Wang Q, Sun Y, Brown C, Tiedje J . FunGene: the functional gene pipeline and repository. Front Microbiol. 2013; 4:291. PMC: 3787254. DOI: 10.3389/fmicb.2013.00291. View

10.

Truu M, Ostonen I, Preem J, Lohmus K, Nolvak H, Ligi T . Elevated Air Humidity Changes Soil Bacterial Community Structure in the Silver Birch Stand. Front Microbiol. 2017; 8:557. PMC: 5376589. DOI: 10.3389/fmicb.2017.00557. View

11.

Zhang Y, Sun Y . HMM-FRAME: accurate protein domain classification for metagenomic sequences containing frameshift errors. BMC Bioinformatics. 2011; 12:198. PMC: 3115854. DOI: 10.1186/1471-2105-12-198. View

12.

Johansen J, Nielsen P, Binnerup S . Identification and potential enzyme capacity of flavobacteria isolated from the rhizosphere of barley (Hordeum vulgare L.). Can J Microbiol. 2009; 55(3):234-41. DOI: 10.1139/w08-116. View

13.

Hu Y, Satten G . Testing hypotheses about the microbiome using the linear decomposition model (LDM). Bioinformatics. 2020; 36(14):4106-4115. PMC: 8453243. DOI: 10.1093/bioinformatics/btaa260. View

14.

Cantarel A, Pommier T, Desclos-Theveniau M, Diquelou S, Dumont M, Grassein F . Using plant traits to explain plant-microbe relationships involved in nitrogen acquisition. Ecology. 2015; 96(3):788-99. DOI: 10.1890/13-2107.1. View

15.

Hamonts K, Clough T, Stewart A, Clinton P, Richardson A, Wakelin S . Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat. FEMS Microbiol Ecol. 2012; 83(3):568-84. DOI: 10.1111/1574-6941.12015. View

16.

Domeignoz-Horta L, Spor A, Bru D, Breuil M, Bizouard F, Leonard J . The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system. Front Microbiol. 2015; 6:971. PMC: 4585238. DOI: 10.3389/fmicb.2015.00971. View

17.

Shcherbak I, Millar N, Robertson G . Global metaanalysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci U S A. 2014; 111(25):9199-204. PMC: 4078848. DOI: 10.1073/pnas.1322434111. View

18.

Bziuk N, Maccario L, Straube B, Wehner G, Sorensen S, Schikora A . The treasure inside barley seeds: microbial diversity and plant beneficial bacteria. Environ Microbiome. 2021; 16(1):20. PMC: 8554914. DOI: 10.1186/s40793-021-00389-8. View

19.

Morrissey E, Mau R, Schwartz E, Caporaso J, Dijkstra P, van Gestel N . Phylogenetic organization of bacterial activity. ISME J. 2016; 10(9):2336-40. PMC: 4989319. DOI: 10.1038/ismej.2016.28. View

20.

Powell J, Karunaratne S, Campbell C, Yao H, Robinson L, Singh B . Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat Commun. 2015; 6:8444. PMC: 4600744. DOI: 10.1038/ncomms9444. View