Skip to main content
Log in

Microbial co-occurrence network in the rhizosphere microbiome: its association with physicochemical properties and soybean yield at a regional scale

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Microbial communities in the rhizosphere play a crucial role in determining plant growth and crop yield. A few studies have been performed to evaluate the diversity and co-occurrence patterns of rhizosphere microbiomes in soybean (Glycine max) at a regional scale. Here, we used a culture-independent method to compare the bacterial communities of the soybean rhizosphere between Nebraska (NE), a high-yield state, and Oklahoma (OK), a low-yield state. It is well known that the rhizosphere microbiome is a subset of microbes that ultimately get colonized by microbial communities from the surrounding bulk soil. Therefore, we hypothesized that differences in the soybean yield are attributed to the variations in the rhizosphere microbes at taxonomic, functional, and community levels. In addition, soil physicochemical properties were also evaluated from each sampling site for comparative study. Our result showed that distinct clusters were formed between NE and OK in terms of their soil physicochemical property. Among 3 primary nutrients (i.e., nitrogen, phosphorus, and potassium), potassium is more positively correlated with the high-yield state NE samples. We also attempted to identify keystone communities that significantly affected the soybean yield using co-occurrence network patterns. Network analysis revealed that communities formed distinct clusters in which members of modules having significantly positive correlations with the soybean yield were more abundant in NE than OK. In addition, we identified the most influential bacteria for the soybean yield in the identified modules. For instance, included are class Anaerolineae, family Micromonosporaceae, genus Plantomyces, and genus Nitrospira in the most complex module (ME9) and genus Rhizobium in ME23. This research would help to further identify a way to increase soybean yield in low-yield states in the U.S. as well as worldwide by reconstructing the microbial communities in the rhizosphere.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Data Availability

The complete 16S rRNA gene sequencing data in this study are available in the National Center for Biotechnology Information (NCBI) database under the BioProject accession number PRJNA873129 associated with the accession numbers of 12 BioSamples (SAMN30489248 - SAMN30489259).

References

  • Barberán, A., Bates, S.T., Casamayor, E.O., and Fierer, N. 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J., 6, 343–351.

    Article  PubMed  Google Scholar 

  • Bastian, M., Heymann, S., and Jacomy, M. 2009. Gephi: an open source software for exploring and manipulating networks. Proc. Int. AAAI Conf. Web Soc. Media, 3, 361–362. Retrieved from https://ojs.aaai.org/index.php/ICWSM/article/view/13937.

    Article  Google Scholar 

  • Becerra-Rivera, V.A. and Dunn, M.F. 2019. Polyamine biosynthesis and biological roles in rhizobia. FEMS Microbiol. Rev., 366, fnz084.

    Article  CAS  Google Scholar 

  • Berry, D. and Widder, S. 2014. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front. Microbiol., 5, 219.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bokulich, N.A., Kaehler, B.D., Rideout, J.R., Dillon, M., Bolyen, E., Knight, R., Huttley, G.A., and Caporaso, J.G. 2018. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin. Microbiome, 6, 90.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolyen, E., Rideout, J.M., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al Ghalith, A.G., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., et al. 2018. QIIME 2: reproducible, interactive, scalable, and extensible microbiome data science. Nat. Biotechnol., 37, 852–857.

    Article  Google Scholar 

  • Boukhatem, Z.F., Merabet, C., and Tsaki, H. 2022. Plant growht promoting actinobacteria, the most promising candidates as bioinoculants?. Front. Agron., 4, 849911.

    Article  Google Scholar 

  • Cao Y. 2022. Package ‘microbiomeMarker’: microbiome biomarker analysis toolkit. R package version 1.2.2. https://github.com/yiluheihei/microbiomeMarker.

    Google Scholar 

  • Chi, S.C., Mothersole, D.J., Dilbeck, P., Niedzwiedzki, D.M., Zhang, H., Qian, P., Vasilev, C., Grayson, K.J., Jackson, P.J., Martin, E.C., et al. 2015. Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway. Biochim. Biophys. Acta, 1847, 189–201.

    Article  CAS  PubMed  Google Scholar 

  • Chowdhury, C., Sinha, S., Chun, S., Yeates, T.O., and Bobik, T.A. 2014. Diverse bacterial microcompartment organelles. Microbiol. Mol. Biol. Rev., 78, 438–468.

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke, K.R. and Ainsworth, M. 1993. A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser., 92, 205–219.

    Article  Google Scholar 

  • Collins, M.D. and Jones, D. 1981. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implications. Microbiol. Rev., 45, 316–354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Csárdi, G. and Nepusz, T. 2006. The igraph software package for complex network research. InterJ. Complex Syst., 1695, 1–9.

    Google Scholar 

  • Cram, J.A., Xia L.C., Needham D.M., Sachdeva R., Sun F., and Fuhrman J.A. 2015. Cross-depth analysis of marine bacterial networks suggests downward propagation of temporal changes. ISME J., 9, 2573–2586.

    Article  PubMed  PubMed Central  Google Scholar 

  • de Menezes, A.B., Prendergast-Miller, M.T., Richardson, A.E., Toscas, P., Farrell, M., Macdonald, L.M., Baker, G., Wark, T., and Thrall, P.H. 2015. Network analysis reveals that bacteria and fungi form modules that correlate independently with soil parameters. Environ. Microbiol., 17, 2677–2689.

    Article  CAS  PubMed  Google Scholar 

  • Ding, B., Niu, J., Shang, F., Yang, L., Chang, T., and Wang, J. 2019. Characterization of the geranylgeranyl diphosphate synthase gene in Acyrthosiphon pisum (Hemiptera: Aphididae) and its association with carotenoid biosynthesis. Front. Physiol., 10, 1398.

    Article  PubMed  PubMed Central  Google Scholar 

  • Douglas, G.M., Maffei, V.J., Zaneveld, J., Yurgel, S.N., Brown, J.R., Taylor, C.M., Huttenhower, C., Langille, M.G.I. 2020. PICRUSt2: an improved and extensible approach for metagenome inference. Nat. Biotechnol., 38, 685–688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Tarabily, K., AlKhajeh, A.S., Ayyash, M.M., Alnuaimi, L.H., Sham, A., ElBaghdady, K.Z., Tariq, S., and AbuQamar, S.F. 2019. Growth promotion of Salicornia bigelovii by Micromonospora chalcea UAE1, and endophytic 1-aminocyclopropane-1-carboxylic acid deaminase-producing actinobacterial isolate. Front. Microbiol., 10, 1694.

    Article  PubMed  PubMed Central  Google Scholar 

  • Expósito, R.G., Postma, J., Raaijmakers, J.M., and Bruijn, I.D. 2015. Diversity and activity of Lysobacter species from disease suppressive soils. Front. Microbiol., 6, 1243.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fierer, N. and Jackson, R.B. 2006. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA, 103, 626–631.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann, A., Rothballer, M., and Schmid, M. 2008. Lorenz Hiltner; a pioneer in rhizosphere microbial ecology & soil bacteriology research. Plant Soil, 312, 7–14.

    Article  CAS  Google Scholar 

  • Herridge, D.F., Peoples, M.B., and Boddey, R.M. 2008. Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil, 311, 1–18.

    Article  CAS  Google Scholar 

  • Hobley, L., Kim, S.H., Maezato, Y., Wyllie, S., Fairlamb, A.H., Stanley-Wall, N.R., and Michael, A.J. 2014. Norspermidine is not a selfproduced trigger for biofilm disassembly. Cell, 156, 844–854.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiménez, J.A., Novinscak, A., and Filion, M. 2020. Inoculation with plant-growth-promoting rhizobacterium Pseudomonas fluorescens LBUM677 impacts the rhizosphere microbiome of three oilseed crops. Front. Microbiol., 11, 569366.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin, D., Kong, X., Li, H., Luo, L., Zhuang, X., Zhuang, G., Deng, Y., and Bai, Z. 2016. Patulibacter brassicae sp. nov., isolated from rhizosphere soil of chinese cabbage (Brassica campestris). Int. J. Syst. Evol. Microbiol., 66, 5056–5060.

    Google Scholar 

  • Jin, J., Wang, G.H., Liu, X.B., Liu, J.D., Chen, X.L., and Herbert, S.J. 2009. Temporal and spatial dynamics of bacterial community in the rhizosphere of soybean genotypes grown in a black soil. Pedosphere, 19, 808–816.

    Article  CAS  Google Scholar 

  • Katoh, K., Misawa, K., Kuma, K., and Miyata, T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res., 30, 3059–3066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Killiny, N. and Nehela, Y. 2020. Citrus polyamines: structure, biosynthesis, and physiological functions. Plants, 9, 426.

    Article  CAS  PubMed Central  Google Scholar 

  • Kim, H.S., Kim, Y.H., Yoo, O.J., and Lee, J.J. 1996. Aclacinomycin X, a novel anthracycline antibiotic produced by Streptomyces galilaeus ATCC 31133. Biosci. Biotech. Biochem., 60, 906–908.

    Article  CAS  Google Scholar 

  • Kraut-Cohen, J., Shapiro, O.H., Dror, B., and Cytryn, E. 2021. Pectin induced colony expansion of soil-derived Flavobacterium strains. Front. Microbiol., 12, 651891.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuffner, M., Puschenreiter, M., Wieshammer, G., Gorfer, M., and Sessitsch, A. 2008. Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil, 304, 35–44.

    Article  CAS  Google Scholar 

  • Langfelder, P. and Horvath, S. 2008. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.

    Article  PubMed  PubMed Central  Google Scholar 

  • Langille, M.G.I., Zaneveld, J., Caporaso, J.G., McDonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Thurber, R.L.V., Knight, R., et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol., 31, 814–821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lankau, R.A., George, I., and Miao, M. 2022. Crop performance is predicted by soil microbial diversity across phylogenetic scales. Ecosphere, 13, e4029.

    Article  Google Scholar 

  • Liang, J., Sun, S., Ji, J., Wu, H., Meng, F., Zhang, M., Zheng, X., Wu, C., and Zhang, Z. 2014. Comparison of the rhizosphere bacterial communities of zigongdongdou soybean and a high-methionine transgenic line of this cultivar. PLoS ONE, 9, e103343.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, C., Sun, Z., Shen, S., Lin, L., Li, T., Tian, B., and Hua, Y. 2013. Identification and characterization of the geranylgeranyl diphosphate synthase in Deinococcus radiodurans. Lett. Appl. Microbiol., 58, 219–224.

    Article  PubMed  Google Scholar 

  • Lozupone, C.A., Hamady, M., Kelley, S.T., and Knight, R. 2007. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol., 73, 1576–1585.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lozupone, C., Lladser, M., Knights, D., Stombaugh, J., and Knight, R. 2011. UniFrac: an effective distance metric for microbial community comparison. ISME J., 5, 169–172.

    Article  PubMed  Google Scholar 

  • Luster, J., Göttlein, A., Nowack, B., and Sarret, G. 2009. Sampling, defining, characterising and modeling the rhizosphere-the soil science tool box. Plant Soil, 321, 457–482.

    Article  CAS  Google Scholar 

  • Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Res., 27, 209–220.

    CAS  PubMed  Google Scholar 

  • Mcdonald, D., Price, M.N., Goodrich, J., Nawrocki, E.P., DeSantis, T.Z., Probst, A., Andersen, G.L., Knight, R., and Hugenholtz, P. 2012. An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME, J. 6, 610–618.

    Article  Google Scholar 

  • Mehrani, M., Sobotka, D., Kowal, P., Ciesielski, S., and Makinia, J. 2020. The occurrence and role of Nitrospiria in nitrogen removal systems. Bioresour. Technol., 303, 122936.

    Article  CAS  PubMed  Google Scholar 

  • Mendes, L.W., Kuramae, E.E., Navarrete, A.A., van Veen, J.A., and Tsai, S.M. 2014. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J., 8, 1577–1587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng, J., Xu, Y., Li, S., Li, C., Zhang, X., Dong, D., and Chen, P. 2010. Soybean growth and soil microbial populations under conventional and conservational tillage systems. J. Crop Improv., 24, 337–348.

    Article  Google Scholar 

  • Mizrahi-Man, O., Davenport, E.R., and Gilad, Y. 2013. Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: evaluation of effective study designs. PLoS ONE, 8, e53608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naik, D., Smith, E., and Cumming, J.R. 2009. Rhizosphere carbon deposition, oxidative stress and nutritional changes in two poplar species exposed to aluminum. Tree Physiol., 29, 423–436.

    Article  CAS  PubMed  Google Scholar 

  • Naim, M.S. 1965. Development of rhizosphere and rhizoplane microflora of Aristida coerulescens in the Libyan desert. Archiv. Mikrobiol., 50, 321–325.

    Article  Google Scholar 

  • Newman, M.E.J. and Girvan, M. 2004. Finding and evaluating community structure in networks. Phys. Rev. E 69, 026113.

    Article  CAS  Google Scholar 

  • Niraula, S., Choi, Y.K., Payne, K., Muir, J.P., Kan, E., and Chang, W.S. 2021. Dairy effluent-saturated biochar alters microbial communities and enhances bermudagrass growth and soil fertility. Agronomy, 11, 1794.

    Article  CAS  Google Scholar 

  • Nowicka, B. and Kruk, J. 2010. Occurrence, biosynthesis and function of isoprenoid quinones. Biochim. Biophys. Acta, 1797, 1587–1605.

    Article  CAS  PubMed  Google Scholar 

  • Park, D., Kim, H., and Yoon, S. 2017. Nitrous oxide reduction by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27. Appl. Environ. Microbiol., 83, e00502–17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Parveen, N. and Cornell, K.A. 2011. Methylthioadenosine/S-adenosylhomocystein nucleosidase, a critical enzyme for bacterial metabolism. Mol. Microbiol., 79, 7–20.

    Article  CAS  PubMed  Google Scholar 

  • Philippot, L., Raaijmakers, J.M., Lemanceau, P., and van der Putten, W.H. 2013. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol., 11, 789–799.

    Article  CAS  PubMed  Google Scholar 

  • Pinda, E.S., Silva, D.B., Teixeira, S.P., Coppede, J.S., Furlan, M., França, S.C., Lopes, N.P., Pereira, A.M.S., and Lopes, A.A. 2016. Mevalonate-derived quinonemethide triterpenoid from in vitro roots of Peritassa laevigata and their localization in root tissue by MALDI imaging. Sci. Rep., 6, 22627.

    Article  Google Scholar 

  • Price, M.N., Dehal, P.S., and Arkin, A.P. 2010. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE, 5, e9490.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rascovan, N., Carbonetto, B., Perrig, D., Díaz, M., Canciani, W., Abalo, M., Alloati, J., González-Anta, G., and Vazquez, M.P. 2016. Integrated analysis of root microbiomes of soybean and wheat from agricultural fields. Sci. Rep., 6, 28084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Röttjers, L. and Faust, K. 2018. From hairballs to hypotheses-biological insights from microbial networks. FEMS Microbiol. Rev., 42, 761–780.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salvagiotti, F., Cassman, K.G., Specht, J.E., Walters, D.T., Weiss, A., and Dobermann, A. 2008. Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crops Res., 108, 1–13.

    Article  Google Scholar 

  • Sang, M.K. and Kim, K.D. 2012. The volatile-producing Flavobacterium johnsoniae strain GDE09 shows biocontrol activity against Phytopthora capsici in pepper. J. Appl. Microbiol., 113, 383–398.

    Article  CAS  PubMed  Google Scholar 

  • Segata, N., Waldron, L., Ballarini, A., Narasimhan, V., Jousson, O., and Huttenhower, C. 2012. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat. Methods, 9, 811–814.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekowska, A., Dénervaud, V., Ashida, H., Michoud, K., Haas, D., Yokota, A., and Danchin, A. 2004. Bacterial variations on the methionine salvage pathway. BMC Microbiol., 4, 9.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spearman, C. 1904. The proof and measurement of association between two things. Am. J. Psychol., 15, 72–101.

    Article  Google Scholar 

  • Staib, L. and Fuchs, T.M. 2015. Regulation of fucose and 1,2-propanedioll utilization by Salmonella enterica serovar Typhimurium. Front. Microbiol., 6, 1116.

    Article  PubMed  PubMed Central  Google Scholar 

  • Strous, M., Fuerst, J.A., Kramer, E.H.M., Logemann, S., Muyzer, G., van de Pas-Schoonen, K.T., Webb, R., Kuenen, J.G., and Jetten, M.S.M. 1999. Missing lithotroph identified as new planctomycete. Nature, 400, 446–449.

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama, A. 2019. The soybean rhizosphere: metabolites, microbes, and beyond-a review. J. Adv. Res., 19, 67–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama, A., Ueda, Y., Zushi, T., Takase, H., and Yazaki, K. 2014. Changes in the bacterial community of soybean rhizospheres during growth in the field. PLoS ONE, 9, e100709.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tao, Y., Bu, C., Zou, L., Hu, Y., Zheng, Z., and Ouyang, J. 2021. A comprehensive review on microbial production of 1,2-proanediol: micro-organisms, metabolic pathways, and metabolic engineering. Biotechnol. Biofuels, 14, 216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao, J., Meng, D., Qin, C., Liu, X., Liang, Y., Xiao, Y., Liu, Z., Gu, Y., Li, J., and Yin, H. 2018. Integrated network analysis reveals the importance of microbial interactions for maize growth. Appl. Microbiol. Biotechnol., 102, 3805–3818.

    Article  CAS  PubMed  Google Scholar 

  • Timm, C.M., Campbell, A.G., Utturkar, S.M., Jun, S., Parales, R.E., Tan, W.A., Robeson, M.S., Lu, T.S., Jawdy, S., Brown, S.D., et al. 2015. Metabolic functions of Pseudomonas fluorescens strains from Populus deltoids depend on rhizosphere or endosphere isolation compartment. Front. Microbiol., 6, 1118.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, R., Zhang, S., Ye, Y., Yu, Z., Qi, H., Zhang, H., Xue, Z., Wang, J., and Wu, M. 2019. Three new isoflavonoid glycosides from the mangrove-derived actinomycete Micromonospora aurantiaca 110B. Mar. Drugs, 17, 294.

    Article  CAS  PubMed Central  Google Scholar 

  • Woese, C.R. 1987. Bacterial evolution. Microbiol. Rev., 51, 221–271.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wotanis, C.K., Brennan, W.P. 3rd, Angotti, A.D., Villa, E.A., Zayner, J.P., Mozina, A.N., Rutkovsky, A.C., Sobe, R.C., Bond, W.G., and Karatan, E. 2017. Relative contributions of norspermidine synthesis and signaling pathways to the regulation of Vibrio cholera biofilm formation. PLoS ONE, 12, e0186291.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, B., Zhang, J., Liu, Y., Shi, P., and Wei, G. 2018. Co-occurrence patterns of soybean rhizosphere microbiome at a continental scale. Soil Biol. Biochem., 118, 178–186.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Genomic Sequencing and Analysis Facility (GSAF) at the University of Texas at Austin for sequencing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Woo-Suk Chang.

Additional information

Conflict of Interest

The authors have no conflict of interest to report.

Electric Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Niraula, S., Rose, M. & Chang, WS. Microbial co-occurrence network in the rhizosphere microbiome: its association with physicochemical properties and soybean yield at a regional scale. J Microbiol. 60, 986–997 (2022). https://doi.org/10.1007/s12275-022-2363-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-022-2363-x

Keywords

Navigation