Abstract
Microbial communities in rhizosphere and endosphere play a pivotal role in plant ecosystems. However, the microbial diversity and community composition of different compartments from Cyperus esculentus L. var. Sativus (C. esculentus L.) remain largely unknown. Four plant compartments were collected at two cultivars from C. esculentus L. and the 16 s rRNA and ITS amplicon sequencing was employed for revealing the microbiomes related to diverse plant compartments. The results indicated that the effect of cultivars on bacterial and fungal abundance was not significant, except for “Round grain stem” and “Long grain stem” samples. The bacterial and fungal α-diversity within “Rhizosphere soil” showed significant differences compared with additional plant compartments. The result of principal coordinate analysis (PCoA) showed that both bacterial and fungal compositions were obviously affected by plant compartments. Gammaproteobacteria and Dothideomycetes abundance of “Stem” was the highest among other plant compartments and bulk soil, whereas Actinobacteria and Sordariomycetes showed the lowest abundance. Thermoleophilia, Pezizomycetes, and Chytridiomycetes were significantly enriched in “Rhizosphere soil.” “Root” had higher relative abundance of Alphaproteobacteria and Agaricomycetes, whereas Tremellomycetes were significantly decreased. Bacteroidia and Agaricomycetes were significantly enriched in “Seed.” Finally, the functional features of bacterial and fungal communities associated with plant compartments of C. esculentus L. were determined. Findings in the present work shed light on the composition and function of microorganisms in different compartments of C. esculentus L. As such, it provided a basis for further studying the interaction mechanism between microbial community and plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams RI, Miletto M, Taylor JW, Bruns TD (2013) Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. ISME J 7:1262–1273. https://doi.org/10.1038/ismej.2013.28
Ayeh-Kumi PF, Tetteh-Quarcoo PB, Duedu KO, Obeng AS, Addo-Osafo K, Mortu S, Asmah RH (2014) A survey of pathogens associated with Cyperus esculentus L (tiger nuts) tubers sold in a Ghanaian city. BMC Res Notes 7:343. https://doi.org/10.1186/1756-0500-7-343
Bado S, Bazongo P, Son G, Kyaw MT, Imal Henri Nestor Bassolé (2015) Physicochemical characteristics and composition of three morphotypes of cyperus esculentus tubers and tuber oils. J Anal Methods Chem 2015, (2015–10–11), 2015(ID 673547). https://doi.org/10.1155/2015/673547
Bao SD (2000) Soil and agricultural chemistry analysis. China Agriculture Press, Beijing, China
Beckers B, Op De Beeck M, Thijs S, Truyens S, Weyens N, Boerjan W, Vangronsveld J (2016) Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Front Microbiol 7(MAY). https://doi.org/10.3389/fmicb.2016.00650
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bredow C, Azevedo JL, Pamphile J, Mangolin C, Rhoden S (2015) In silico analysis of the 16S rRNA gene of endophytic bacteria, isolated from the aerial parts and seeds of important agricultural crops. Genet Mol Res 14:9703–9721. https://doi.org/10.4238/2015.August.19.3
Bulgarelli D, Rott M, Schlaeppi K, Loren V, van Themaat E, Ahmadinejad N, Assenza F, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488(7409):91–95. https://doi.org/10.1038/nature11336
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17(3):392–403. https://doi.org/10.1016/j.chom.2015.01.011
Chen L, Shi H, Heng JY, Wang DX, Bian K (2019) Antimicrobial, plant growth-promoting and genomic properties of the peanut endophyte Bacillus velezensis LDO2. Microbiol Res 218:41–48. https://doi.org/10.1016/j.micres.2018.10.002
Chen P, Zhao M, Tang F, Hu Y, Shen S (2020) The effect of plant compartments on the broussonetia papyrifera-associated fungal and bacterial communities. Appl Microbiol Biot 104(7582). https://doi.org/10.1007/s00253-020-10466-6
Citlali F-G, Devin CD, Etzel G, Axel V, Tringe SG, Partida-Martínez Laila P (2016) The cacti microbiome: interplay between habitat-filtering and host-specificity. Front Microbiol 7:150. https://doi.org/10.3389/fmicb.2016.00150
Coleman-Derr D Desgarennes D Fonseca-Garcia C Gross S Clingenpeel S Woyke T North G Visel A Partida-Martinez LP Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New phytol 209. https://doi.org/10.1111/nph.13697
Cui JL, Wang CL, Guo SX, Xiao PG, Wang ML (2013) Stimulation of dragon’s blood accumulation in Dracaena cambodiana via fungal inoculation. Fitoterapia 87:31–36. https://doi.org/10.1016/j.fitote.2013.03.012
Deangelis KM, Brodie EL, Desantis TZ, Andersen GL, Firestone MK (2009) Selective progressive response of soil microbial community to wild oat roots. Isme J 3(2):168–178. https://doi.org/10.1038/ismej.2008.103
Desgarennes D, Garrido E, Torres-Gomez MJ, Pena-Cabriales JJ, Partida-Martinez LP (2014) Diazotrophic potential among bacterial communities associated with wild and cultivated Agave species. FEMS Microbiol Ecol 90(3):844–857. https://doi.org/10.1111/1574-6941.12438
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Edwards J Johnson C Santos-Medellín C Lurie E Podishetty N Bhatnagar S Eisen J Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112. https://doi.org/10.1073/pnas.1414592112
Fonseca-García Citlali, Devin CD, Etzel G, Axel V, Tringe SG, Partida-Martínez Laila P (2016) The cacti microbiome: interplay between habitat-filtering and host-specificity. Frontiers in Microbiology 7:150
Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M, Karpinets T, Uberbacher E, Tuskan GA, Vilgalys R, Doktycz MJ, Schadt CW (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol Sep 77(17): 5934–44. https://doi.org/10.1128/AEM.05255-11
Hallmann J, Berg G (2006) Spectrum and population dynamics of bacterial root endophytes. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial Root Endophytes. Soil Biol, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-33526-9_2
Hameed A, Yeh MW, Hsieh YT, Chung WC, Lo CT, Young LS (2015) Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L.) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress. Plant Soil 394:177–197. https://doi.org/10.1007/s11104-015-2506-5
Holm LG, Plucknett DL, Pancho JV, Herberger PJ (1977) The world’s worst weeds: distribution and biology. University Press of Hawaii, Honolulu, Hawaii, USA
Huygh W, Larridon I, Reynders M, Muasya AM, Govaerts R, Simpson DA, Goetghebeur P (2010) Nomenclature and typification of names of genera and subdivisions of genera in Cypereae (Cyperaceae): 1. Names of genera in the Cyperus clade. Taxon 59:1883–1890. https://doi.org/10.1002/tax.596021
Ji P, Rhoads WJ, Edwards MA, Pruden A (2018) Effect of heat shock on hot water plumbing microbiota and Legionella pneumophila control. Microbiome 6:30. https://doi.org/10.1186/s40168-018-0406-7
Jing SQ, Wang SS, Li Q, Zheng L, Yue L, Fan SL, Tao GJ (2016) Dynamic high pressure microfluidization-assisted extraction and bioactivities of Cyperus esculentus (C. esculentus L.) leaves flavonoids. Food Chem 192:319–327. https://doi.org/10.1016/j.foodchem.2015.06.097
Jing SQ, Wang SS, Zhong RM, Zhang JY, Wu JZ, Tu YX, Pu Y, Yan LJ (2020) Neuroprotection of Cyperus esculentus L. orientin against cerebral ischemia/reperfusion induced brain injury. Neural Regen Res 15(3): 548–556. https://doi.org/10.4103/1673-5374.266063
Langille M, Zaneveld J, Caporaso J, McDonald D, Knights D, Reyes J, Clemente J, Burkepile D, Thurber R, Knight R, Beiko R, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Larridon I, Huygh W, Reynders M, Muasya AM, Govaerts R, Simpson DA, Goetghebeur P (2011) Nomenclature and typification of names of genera and subdivisions of genera in Cypereae (Cyperaceae): 2. Names of Subdivisions of Cyperus Taxon 60:868–884. https://doi.org/10.1002/tax.603021
Liotti RG, da Silva Figueiredo MI, da Silva GF, de Mendonça EAF, Soares MA (2018) Diversity of cultivable bacterial endophytes in Paullinia cupana and their potential for plant growth promotion and phytopathogen control. Microbiol Res 207:8–18. https://doi.org/10.1016/j.micres.2017.10.011
Liu H, Carvalhais LC, Schenk PM, Dennis PG (2017a) Effects of jasmonic acid signalling on the wheat microbiome differ between body sites. Sci Rep-Uk 7:41766. https://doi.org/10.1038/srep41766
Liu H Carvalhais LC Crawford M Singh E Dennis PG Pieterse CMJ Schenk PM (2017b) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017b.02552
Lundberg D, Lebeis PS, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. https://doi.org/10.1038/nature11237
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Marcos MS, Bertiller MB, Olivera NL (2019) Microbial community composition and network analyses in arid soils of the Patagonian Monte under grazing disturbance reveal an important response of the community to soil particle size. Appl Soil Ecol 138:223–232. https://doi.org/10.1016/j.apsoil.2019.03.001
Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587. https://doi.org/10.1038/ismej.2014.17
Nacke H, Fischer C, Thürmer A, Meinicke P, Daniel R (2014) Land use type significantly affects microbial gene transcription in soil. Microb Ecol 67:919–930. https://doi.org/10.1007/s00248-014-0377-6
Ntukidem VE, Ukwo PS, Udoh IE, Umoinyang EU (2019) Influence of different pretreatments on the nutritional and organoleptic properties of vegetable milk produced locally from tiger-nut (Cyperus esculentus) tubers. IOSR-JESTFT 13(6):55–61. https://doi.org/10.9790/2402-1306025561
Nyarko HD, Daniel NAT and Yaw A (2011) Assessment of microbiological safety of tiger nuts (Cyperus esculentus L.) in the Cape Coast Metropolis of Ghana. Arch Appl Sci Res 3(6): 257–262
Ottesen AR, González Peña A, White JR, Pettengi JB, Li C, Allard S, Brown E (2013) Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiol 13(1). https://doi.org/10.1186/1471-2180-13-114
Penuelas J, Rico L, Ogaya R, Jump A, Terradas J (2012) Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biol 14:565–575. https://doi.org/10.1111/j.1438-8677.2011.00532.x
Pereira P, Ibáñez F, Rosenblueth M, Etcheverry M, Martínez-Romero E (2011) Analysis of the bacterial diversity associated with the roots of maize (Zea mays L.) through culture-dependent and culture-independent methods. ISRN Ecol 1–10. https://doi.org/10.5402/2011/938546
Schmidt R, Mitchell J, Scow K (2018) Cover cropping and no-till increase diversity and symbiotroph:saprotroph ratios of soil fungal communities. Soil Biol Biochem 129:99–109. https://doi.org/10.1016/j.soilbio.2018.11.010
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6). https://doi.org/10.1186/gb-2011-12-6-r60
Shakya M Gottel N Castro H Yang ZK Gunter L Labbé J Muchero W Gregory V Rytas T (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One 8. https://doi.org/10.1371/journal.pone.0076382
Shi Y, Yang H, Zhang T, Sun J, Lou K (2014) Illumina-based analysis of endophytic bacterial diversity and space-time dynamics in sugar beet on the north slope of Tianshan mountain. Appl Microbiol Biotechnol 98(14):6375–6385. https://doi.org/10.1007/s00253-014-5720-9
Sohn SI, Oh YJ, Kim BY, Cho HS (2016) Effects of CaMSRB2-expressing transgenic rice cultivation on soil microbial communities. J Microbiol Biotechnol 26:1303–1310. https://doi.org/10.4014/jmb.1601.01058
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44(4):846–849. https://doi.org/10.1099/00207713-44-4-846
Strobel G, Stierle A, Stierle D, Hess WM (1993) Taxomyces andreanae new genus new species, a proposed new taxon for a bulbilliferous hyphomycete associated with Pacific yew (Taxus brevifolia). Mycotaxon 47:71–80
Tardif S, Yergeau É, Tremblay J, Legendre P, Whyte LG, Greer CW (2016) The willow microbiome is influenced by soil petroleum-hydrocarbon concentration with plant compartment-specific effects. Front Microbiol 7(SEP). https://doi.org/10.3389/fmicb.2016.01363
Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209. https://doi.org/10.1126/science.aad0092
Upreti R, Thomas P (2015) Root-associated bacterial endophytes from Ralstonia sola nacearum resistant and susceptible tomato cultivars and their pathogen antagonistic effects. Front Microbiol 6:255. https://doi.org/10.3389/fmicb.2015.00255
Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Gilbert JA (2015) The soil microbiome influences grapevine-associated microbiota. MBio 6(2). https://doi.org/10.1128/mBio.02527-14
Funding
This study was supported by the Shanghai Agriculture Applied Technology Development Program (Grant No. 2020–2-1), the National Natural Science Foundation of China (31801511), the Shanghai Agricultural Science and Technology Innovation Action Plan No. 21N31900800, the Shanghai Natural Science Foundation (No. 19ZR1436800), the Shanghai Sailing Program (No. 20YF1443000), the Technology Support Project (No. KJZC202008), the Shanghai Fresh Corn Technology System Project (No. 10 2017), and the SAAS Program for Excellent Research Team (No. 2022 (016)) for financial support to this study.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wang, S., Wang, J., Zhou, Y. et al. Comparative Analysis on Rhizosphere Soil and Endophytic Microbial Communities of Two Cultivars of Cyperus esculentus L. Var. Sativus. J Soil Sci Plant Nutr 22, 2156–2168 (2022). https://doi.org/10.1007/s42729-022-00800-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-022-00800-4