Skip to main content

Advertisement

SpringerLink
Log in

Shifts in the bacterial community along with root-associated compartments of maize as affected by goethite

  • Short Communication
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Root-associated compartments, including rhizosphere soil, rhizoplane soil, and the endosphere, are found to harbor distinguished bacterial populations and community composition, but how microbiome in these rhizo-compartments are affected by edaphic variables remains largely unknown. Goethite is a prevalent crystalline iron (hydr)oxide mineral of the soil matrix and strongly interact with microbial communities. The objective of our study was to determine how goethite (α-FeOOH) amendment assemble bacterial communities in the rhizo-compartments of Maize (Zea mays. L). Using sequencing of microbial 16S ribosomal RNA gene amplicons, we revealed that goethite amendment into soil enriched Actinobacteria and depleted Proteobacteria in all rhizo-compartments. Also, goethite enlarged the differences in the alpha diversity (Chao) between rhizo-compartments, with much lower mean diversity in the endosphere and rhizoplane compared with rhizosphere soil, indicating a higher selection of the microbiome assemblage. This was supported by beta Nearest Taxon Index (βNTI > + 2), indicating that changes in environmental conditions progressively increase the strength of selection. It suggests that variable selection (a deterministic process) was the dominant process influencing the microbial assembly in soil amended with goethite. According to the distance-based linear modeling (distLM), the assemblage of bacterial communities in the rhizosphere compartments was regulated by specific edaphic variables, with the major contributors being goethite (62%), total C (52%), soil pH (50%), and FeOM (25%). Stabilization of rhizosphere C in the presence of goethite would be the selective step for its accessibility and consequent microbial community. For instance, the keystone microorganisms, e.g., Pseudomonas, had more negative links within the goethite added co-occurrence network, indicating its mutual exclusions and outcompete other microbes in C/nutrients limited conditions. Thus, goethite narrows the composition of rhizosphere mainly due to “gate selection” effects on rhizodeposits, which limited microbial penetrance into inner-compartments, consequently assemble the rhizosphere bacterial community via deterministic process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Anderson MJ, Legendre P (1999) An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. J Stat Comput Simul 62:271–303

    Google Scholar 

  • Asadishad B, Ghoshal S, Tufenkji N (2013) Short-term inactivation rates of selected gram-positive and gram-negative bacteria attached to metal oxide mineral surfaces: role of solution and surface chemistry. Environ Sci Technol 47:5729–5737

    PubMed  CAS  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open-source software for exploring and manipulating networks Third international AAAI conference on weblogs and social media Paris, France

  • Bulgarelli D, Rott M, van Schlaeppi K, Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

    PubMed  CAS  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621–1624

  • Carson JK, Campbell L, Rooney D, Clipson N, Gleeson DB (2009) Minerals in soil select distinct bacterial communities in their microhabitats. FEMS Microbiol Ecol 67:381–388

    PubMed  CAS  Google Scholar 

  • Caruso T, Chan Y, Lacap DC, Lau MCY, McKay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413

    PubMed  PubMed Central  Google Scholar 

  • Chen C, Dynes JJ, Wang J, Sparks DL (2014) Properties of Fe-organic matter associations via coprecipitation versus adsorption. Environ Sci Technol 48:13751–13759

    PubMed  CAS  Google Scholar 

  • Chen L, Brookes PC, Xu J, Zhang J, Zhang C, Zhou X, Yu L (2016) Structural and functional differentiation of the root-associated bacterial microbiomes of perennial ryegrass. Soil Biol Biochem 98:1–10

    CAS  Google Scholar 

  • Denison RF, Kiers ET (2004) Lifestyle alternatives for rhizobia: mutualism parasitism and forgoing symbiosis. FEMS Microbiol Lett 237:187–193

    PubMed  CAS  Google Scholar 

  • Dibbern D, Schmalwasser A, Lueders T, Totsche KU (2014) Selective transport of plant root-associated bacterial populations in agricultural soils upon snowmelt. Soil Biol Biochem 69:187–196

    CAS  Google Scholar 

  • Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci U S A 112:E1326–E1332

    PubMed  PubMed Central  CAS  Google Scholar 

  • Doetterl S, Stevens A, Six J, Merckx R, Oost KV, Pinto MC, Casanovakatny A, Muñoz C, Boudin M, Venegas EZ (2015) Soil carbon storage controlled by interactions between geochemistry and climate. Nat Geosci 8:780–783

    CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    PubMed  CAS  Google Scholar 

  • Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure variation and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 112:911–920

    Google Scholar 

  • El Zahar Haichar F, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent JM, Fan K, Cardona C, Li Y, Shi Y, Xiang X, Shen C, Wang H, Gilbert JA, Chu H (2017) Rhizosphere-associated bacterial network structure and spatial distribution differ significantly from bulk soil in wheat crop fields. Soil Biol Biochem 113:275–284

    Google Scholar 

  • Fan K, Cardona C, Li Y, Yu S, Xiang X, Shen C, Wang H, Gilbert JA, Chu H (2017) Rhizosphere-associated bacterial network structure and spatial distribution differ significantly from bulk soil in wheat crop fields. Soil Biol Biochem 113:275–284

  • Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550

    PubMed  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    PubMed  Google Scholar 

  • Freilich S, Zarecki R, Eilam O, Segal ES, Henry CS, Kupiec M, Gophna U, Sharan R, Ruppin E (2011) Competitive and cooperative metabolic interactions in bacterial communities. Nat Commun 2:589

    PubMed  Google Scholar 

  • Ge T, Yu L, He X (2019) Quantitative and mechanistic insights into the key process in the rhizodeposited carbon stabilization, transformation and utilization of carbon, nitrogen and phosphorus in paddy soil. Plant Soil 445(1-2):1–5

  • Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58

    PubMed  PubMed Central  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152

  • Hori T, Müller A, Igarashi Y, Conrad R, Friedrich MW (2010) Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J 4:267–278

    PubMed  CAS  Google Scholar 

  • Jones B, Renaut RW (2007) Selective mineralization of microbes in Fe-rich precipitates (jarosite, hydrous ferric oxides) from acid hot springs in the Waiotapu geothermal area, North Island, New Zealand. Sediment Geol 194:77–98

    CAS  Google Scholar 

  • Kaiser K, Guggenberger G (2007) Sorptive stabilization of organic matter by microporous goethite: sorption into small pores vs surface complexation. Eur J Soil Sci 58:45–59

    CAS  Google Scholar 

  • Karthikeyan N, Prasanna R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30

    CAS  Google Scholar 

  • Li Y, Li Y, Chang SX, Yang Y, Shenglei F, Jiang P, Yu L, Yang M, Chen Z, Hu S, Zhao M, Xue L, Xu Q, Zhou G, Zhou J (2018) Biochar reduces soil heterotrophic respiration in a subtropical plantation through increasing soil organic carbon recalcitrancy and decreasing carbon-degrading microbial activity. Soil Biol Biochem 122:173–185

  • Liu H, Yu D, Zhang Q, Liu X, Xu J, Li Y, Di H (2019) Heterotrophic nitrification and denitrification are the main sources of nitrous oxide in two paddy soils. Plant Soil 445(1-2):39–53

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    PubMed  PubMed Central  Google Scholar 

  • Lugtenberg BJ, Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1:9–13

    PubMed  CAS  Google Scholar 

  • Luo Y, Zhu Z, Liu S, Peng P, Xu J, Brookes P, Ge T, Wu J (2019) Nitrogen fertilization increases rice rhizodeposition and its stabilization in soil aggregates and the humus fraction. Plant Soil 445:125–135

    CAS  Google Scholar 

  • Ma W, Peng D, Walker SL, Cao B, Gao CH, Huang Q, Cai P (2017) Bacillus subtilis biofilm development in the presence of soil clay minerals and iron oxides. Biofilms Microbiol 3:4

    Google Scholar 

  • Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nannipieri P, Ascher-Jenull J, Ceccherini MT, Pietramellara G, Renella G, Schloter M (2020) Beyond microbial diversity for predicting soil functions: a mini review. Pedosphere 30:5–17

    Google Scholar 

  • Nuccio EE, Anderson-Furgeson J, Estera KY, Pett-Ridge J, de Valpine P, Brodie EL, Firestone MK (2016) Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. Ecology 97:1307–1318

    PubMed  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Com Ecol Pack 10:631–637

    Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Pii Y, Borruso L, Brusetti L, Crecchio C, Cesco S, Mimmo T (2016) The interaction between iron nutrition plant species and soil type shapes the rhizosphere microbiome. Plant Physiol Biochem 99:39–48

    PubMed  CAS  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    PubMed  Google Scholar 

  • Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87

    PubMed  PubMed Central  Google Scholar 

  • Schreiter S, Ding GC, 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

    PubMed  PubMed Central  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:60

    Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    PubMed  PubMed Central  CAS  Google Scholar 

  • Silva-Lacerda G, Santana R, Vicalvi-Costa M, Solidônio E, Sena K, Lima G, Araújo J (2016) Antimicrobial potential of actinobacteria isolated from the rhizosphere of the Caatinga biome plant Caesalpinia pyramidalis Tul. Genet Mol Res 15:1–12

    Google Scholar 

  • Somenahally AC, Hollister EB, Yan W, Gentry TJ, Loeppert RH (2011) Water management impacts on arsenic speciation and iron-reducing bacteria in contrasting rice-rhizosphere compartments. Environ Sci Technol 45:8328–8335

    PubMed  CAS  Google Scholar 

  • Tyc O, Song C, Dickschat JS, Vos M, Garbeva P (2017) The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol 25:280–292

    PubMed  CAS  Google Scholar 

  • Valverde A, Makhalanyane TP, Cowan DA (2014) Contrasting assembly processes in a bacterial metacommunity along a desiccation gradient. Front Microbiol 5:668

    PubMed  PubMed Central  Google Scholar 

  • Vandenkoornhuyse P, Mahé S, Ineson P, Staddon P, Ostle N, Cliquet J-B, Francez A-J, Fitter AH, JPW Y (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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484

    Google Scholar 

  • Vogel C, Heister K, Buegger F, Tanuwidjaja I, Haug S, Schloter M, Kögel-Knabner I (2015) Clay mineral composition modifies decomposition and sequestration of organic carbon and nitrogen in fine soil fractions. Biol Fertil Soils 51:427–442

    CAS  Google Scholar 

  • Walker TS, Bais HP, Déziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM (2004) Pseudomonas aeruginosa-plant root interactions pathogenicity biofilm formation and root exudation. Plant Physiol 134:320–331

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wan D, Ye T, Lu Y, Chen W, Cai P, Huang Q (2019) Iron oxides selectively stabilize plant-derived polysaccharides and aliphatic compounds in agricultural soils. Eur J Soil Sci 70:1153–1163

    CAS  Google Scholar 

  • Wang H, Wei Z, Mei L, Gu J, Yin S, Faust K, Raes J, Deng Y, Wang Y, Shen Q (2017) Combined use of network inference tools identifies ecologically meaningful bacterial associations in a paddy soil. Soil Biol Biochem 105:227–235

    CAS  Google Scholar 

  • Wei X, Zhu Z, Liang W, Wu J, Ge T (2019a) Biogeochemical cycles of key elements in the paddy-rice rhizosphere: Microbial mechanisms and coupling processes. Rhizosphere 10:100145

  • Wei X, Razavi BS, Hu Y, Xu X, Zhu Z, Liu Y, Kuzyakov Y, Li Y, Wu J, Ge T (2019b) C/P stoichiometry of dying rice root defines the spatial distribution and dynamics of enzyme activities in root-detritusphere. Biol Fertil Soils 55(3):251–263

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    PubMed  CAS  Google Scholar 

  • Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to bacyerial abundance and plant iron nutritional status. Appl Environ Microbiol 66:345–351

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yu Z, Chen L, Pan S, Li Y, Kuzyakov Y, Xu J, Brookes PC, Luo Y (2018) Feedstock determines biochar-induced soil priming effects by stimulating the activity of specific microorganisms. Eur J Soil Sci 69(3):521–534

  • Yu G, Xiao J, Hu S, Polizzotto ML, Zhao F, McGrath SP, Li H, Ran W, Shen Q (2017) Mineral availability as a key regulator of soil carbon storage. Environ Sci Technol 51:4960–4969

    PubMed  CAS  Google Scholar 

  • Zhang C, Song Z, Zhuang, D, Wang J, Xie S, Liu G (2019) Urea fertilization decreases soil bacterial diversity, but improves microbial biomass, respiration, and N-cycling potential in a semiarid grassland. Biol Fertil Soils 55:229–242

Download references

Funding

This work was supported by the National Natural Science Foundation of China (41671233 41721001 41807017).

Author information

Author notes

  1. Peduruhewa H Jeewani and Lin Chen contributed equally to this work.

Authors and Affiliations

  1. Institute of Soil and Water Resources and Environmental Science, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou, 310058, China

    Peduruhewa H Jeewani, Yu Luo & Jianming Xu

  2. Department of Agriculture, Southern Province, Galle, 80000, Sri Lanka

    Peduruhewa H Jeewani

  3. State Key Laboratory of Soil and Sustainable Agriculture Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Lin Chen

  4. NSW Department of Primary Industries, Wollongbar Primary Industries Institute, Wollongbar, NSW, 2477, Australia

    Lukas Van Zwieten

  5. Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Congcong Shen

  6. Institute of Soil Science, Leibniz Universität Hannover, 30419, Hannover, Germany

    Georg Guggenberger

Authors
  1. Peduruhewa H Jeewani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lukas Van Zwieten
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Congcong Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Georg Guggenberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianming Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yu Luo.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 1306 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeewani, P.H., Chen, L., Van Zwieten, L. et al. Shifts in the bacterial community along with root-associated compartments of maize as affected by goethite. Biol Fertil Soils 56, 1201–1210 (2020). https://doi.org/10.1007/s00374-020-01458-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-020-01458-9

Keywords

Search

Navigation