Abstract
This study aims to investigate the effects of soil as a microbial source on the assemblage of the endophytic bacterial communities in rice roots. Rice seedlings were grown hydroponically with the addition of a permeable bag filled with one of five soil types collected from different geographical locations in Japan. After 3 and 6 weeks, the endophytic bacterial communities in rice roots were analyzed using the Illumina Miseq-based 16SrRNA gene amplicon sequencing method. The results showed that the bacterial community in the soils added as a microbial source differed among the soil types, which affected the bacterial community in the hydroponic solution and consequently reflected in the endophytic bacterial community assemblage. Bacterial diversity and richness differed significantly with respect to the microbial sources. As a result, a conserved group of 16 endophytic bacterial taxa at the genus level, dominated by Burkholderia-Caballeronia-Paraburkholderia, and independent of the soil type were shared across all microbial sources, thereby underlining the ability of rice plants to selectively recruit their endophytic inhabitants. Altogether, this study demonstrates the importance of the microbial source as a crucial driving force for the formation of the endophytic bacterial communities in rice roots.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The raw 16S rRNA gene amplicon sequence data for this study were deposited in the DDBJ under the following accession number: DRA015220.
References
Ali M, Ali Q, Sohail MA, Ashraf MF, Saleem MH, Hussain S, Zhou L (2021) Diversity and taxonomic distribution of endophytic bacterial community in the rice plant and its prospective. Int J Mol Sci 22:10165. https://doi.org/10.3390/ijms221810165
Asiloglu R, Shiroishi K, Suzuki K, Turgay OC, Murase J, Harada N (2020) Protist-enhanced survival of a plant growth promoting rhizobacteria, Azospirillum sp. B510, and the growth of rice (Oryza sativa L) plants. Appl Soil Ecol 154:103599. https://doi.org/10.1016/j.apsoil.2020.103599
Bach EM, Williams RJ, Hargreaves SK, Yang F, Hofmockel KS (2018) Greatest soil microbial diversity found in micro-habitats. Soil Biol Biochem 118:217–226. https://doi.org/10.1016/j.soilbio.2017.12.018
Bai R, Wang JT, Deng Y, He JZ, Feng K, Zhang LM (2017) Microbial community and functional structure significantly varied among distinct types of paddy soils but responded differently along gradients of soil depth layers. Front Microbiol 8:945. https://doi.org/10.3389/fmicb.2017.00945
Bogas AC, Ferreira AJ, Araújo WL, Astolfi-Filho S, Kitajima EW, Lacava PT, Azevedo JL (2015) Endophytic bacterial diversity in the phyllosphere of Amazon Paullinia cupana associated with asymptomatic and symptomatic anthracnose. Springerplus 4:258. https://doi.org/10.1186/s40064-015-1037-0
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Breidenbach B, Pump J, Dumont MG (2016) Microbial community structure in the rhizosphere of rice plants. Front Microbiol 6:1537. https://doi.org/10.3389/fmicb.2015.01537
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522. https://doi.org/10.1073/pnas.1000080107
Core R Team (2019) A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https:// www.R-project.org. Accessed 20 June 2021
Cui X, Zhang Y, Gao J (2018) Long-term combined application of manure and chemical fertilizer sustained higher nutrient status and rhizospheric bacterial diversity in reddish paddy soil of Central South China. Sci Rep 8:16554. https://doi.org/10.1038/s41598-018-34685-0
Dai JX, Liu XM, Wang YJ (2014) Diversity of endophytic bacteria in Caragana microphylla grown in the desert grassland of the Ningxia Hui Autonomous Region of China. Genet Mol Res 13:2349–2358. https://doi.org/10.4238/2014.April.3.7
Dang H, Zhang T, Li G, Mu Y, Lv X, Wang Z, Zhuang L (2020) Root-associated endophytic bacterial community composition and structure of three medicinal licorices and their changes with the growing year. BMC Microbiol 20:291. https://doi.org/10.1186/s12866-020-01977-3
Ding T, Melcher U (2016) Influences of plant species, season and location on leaf endophytic bacterial communities of non-cultivated plants. PLoS ONE 11:e0150895. https://doi.org/10.1371/journal.pone.0150895
Dwevedi A, Kumar P, Kumar P, Kumar Y, Sharma YK, Kayastha AM (2017) Soil sensors: detailed insight into research updates, significance, and future prospects. In: AM Grumezescu (Ed.) New Pesticides and Soil Sensors. Academic Press 10:561–594. https://doi.org/10.1016/b978-0-12-804299-1.00016-3
Edwards J, Santos-Medellín C, Nguyen B, Kilmer J, Liechty Z, Veliz E, Ni J, Phillips G, Sundaresan V (2019) Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota. Genome Biol 20:221. https://doi.org/10.1186/s13059-019-1825-x
Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato YI, Morisaki H, Mitsui H, Minamisawa K (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nut 46:3. https://doi.org/10.1080/00380768.2000.10409127
Ferrando L, Scavino AF (2015) Strong shift in the diazotrophic endophytic bacterial community inhabiting rice (Oryza sativa) plants after flooding. FEMS Microbiol Ecol 91:9. https://doi.org/10.1093/femsec/fiv104
Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Env Microbiol 13:6. https://doi.org/10.1111/j.1462-2920.2011.02480.x
Guglielmetti S, Basilico R, Taverniti V, Arioli S, Piagnani C, Bernacchi A (2013) Luteibacter rhizovicinus MIMR1 promotes root development in barley (Hordeum vulgare L.) under laboratory conditions. World J Microbiol Biotechnol 29:11. https://doi.org/10.1007/s11274-013-1365-6
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
Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. https://doi.org/10.1016/j.tim.2008.07.008
Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, van Elsas JD (2011) Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol 77:154–164. https://doi.org/10.1111/j.1574-6941.2011.01092.x
Hardoim PR, Hardoim CCP, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7:e30438. https://doi.org/10.1371/journal.pone.0030438
Haygarth PM, Ritz K (2009) The future of soils and land use in the UK: soil systems for the provision of land-based ecosystem services. Land Use Policy 26:S187–S197. https://doi.org/10.1016/j.landusepol.2009.09.016
He H, Pang J, Wu GL, Lambers H (2019) The application potential of coal fly ash for selenium biofortification. Adv Agron 157:1–54. https://doi.org/10.1016/bs.agron.2019.05.002
Hemkemeyer M, Dohrmann AB, Christensen BT, Tebbe CC (2018) Bacterial preferences for specific soil particle size fractions revealed by community analyses. Front Microbiol 9:149. https://doi.org/10.3389/fmicb.2018.00149
IUSS Working Group WRB (2015) World Reference Base for soil resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World soil resources reports No 106. FAO, Rome
Jones JM, Boehm EL, Kahmark K, Lau J, Evans S (2022) Microbial community response to drought depends on crop. Elementa 10:00110. https://doi.org/10.1525/elementa.2021.00110
Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S, Morisaki H (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ 24:154–162. https://doi.org/10.1264/jsme2.ME09113
Kataoka T, Mitsunobu S, Hamamura N (2018) Influence of the chemical form of antimony on soil microbial community structure and arsenite oxidation activity. Microbes Environ 33:214–221. https://doi.org/10.1264/jsme2.ME17182
Kivlin SN, Hawkes CV (2016) Temporal and spatial variation of soil bacteria richness, composition, and function in a neotropical rainforest. PLoS ONE 11:e0159131. https://doi.org/10.1371/journal.pone.0159131
Kononov A, Hishida M, Suzuki K, Harada N (2022) Microplastic extraction from agricultural soils using canola oil and unsaturated sodium chloride solution and evaluation by incineration method. Soil Syst 6:54. https://doi.org/10.3390/soilsystems6020054
Kozaki D, Sago Y, Fujiwara T, Mori M, Kubono C, Koga T, Mitsui Y, Tachibana T (2021) Ion-exclusion/cation-exchange chromatography using dual-ion-exchange groups for simultaneous determination of inorganic ionic nutrients in fertilizer solution samples for the management of hydroponic culture. Agron J 11:1847. https://doi.org/10.3390/agronomy11091847
Kumar U, Shahid M, Tripathi R, Mohanty S, Kumar A, Bhattacharyya P, Lal B, Gautam P, Raja R, Panda BB, Jambhulkar NN, Shukla AK, Nayak AK (2017) Variation of functional diversity of soil microbial community in sub-humid tropical rice-rice cropping system under long-term organic and inorganic fertilization. Ecol Indic 73:536–543. https://doi.org/10.1016/j.ecolind.2016.10.014
Kuramae EE, Yergeau E, Wong LC, Pijl AS, Van Veen JA, Kowalchuk GA (2012) Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol 79:12–24. https://doi.org/10.1111/j.1574-6941.2011.01192.x
Li B, Xu R, Sun X, Han F, Xiao E, Chen L, Qiu L, Sun W (2021) Microbiome-environment interactions in antimony-contaminated rice paddies and the correlation of core microbiome with arsenic and antimony contamination. Chemosphere 263:128227. https://doi.org/10.1016/j.chemosphere.2020.128227
Li C, Yan K, Tang L, Jia Z, Li Y (2014) Change in deep soil microbial communities due to long-term fertilization. Soil Biol Biochem 75:264–272. https://doi.org/10.1016/j.soilbio.2014.04.023
Lin GY, Lin CY, Chang SJ, Lin WY (2020) The dynamics of endophytic bacterial community structure in rice roots under different field management systems. Agron J 10:1623. https://doi.org/10.3390/agronomy10111623
Long HH, Sonntag DG, Schmidt DD, Baldwin IT (2010) The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. New Phytol 185:554–567. https://doi.org/10.1111/j.1469-8137.2009.03079.x
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. https://doi.org/10.1038/nature11237
Luo X, Fu X, Yang Y, Cai P, Peng S, Chen W, Huang Q (2016) Microbial communities play important roles in modulating paddy soil fertility. Sci Rep 6:20326. https://doi.org/10.1038/srep20326
Ma W, Tang S, Dengzeng Z, Zhang D, Zhang T, Ma X (2022) Root exudates contribute to belowground ecosystem hotspots: a review. Front Microbiol 13:937940. https://doi.org/10.3389/fmicb
Mahaffee WF, Kloepper JW (1997) Temporal changes in the bacterial communities of soil, rhizosphere, and endorhiza associated with field-grown cucumber (Cucumis sativus L.). Microb Ecol 34:210–213. https://doi.org/10.1007/s002489900050
Mannaa M, Park I, Seo YS (2019) Genomic features and insights into the taxonomy, virulence, and benevolence of plant-associated Burkholderia species. Int J Mol Sci 20:121. https://doi.org/10.3390/ijms20010121
Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117. https://doi.org/10.1264/jsme2.23.109
Megías AG, Müller C (2010) Root herbivores and detritivores shape above-ground multitrophic assemblage through plant-mediated effects. J Anim Ecol 79:923–931. https://doi.org/10.1111/j.1365-2656.2010.01681.x
Nannipieri P, Penton CR, Purahong W, Schloter M, van Elsas JD (2019) Recommendations for soil microbiome analyses. Biol Fertil Soils 55:765–766. https://doi.org/10.1007/s00374-019-01409-z
Obara H, Maejima Y, Kohyama K, Ohkura T, Takata Y (2015) Outline of the comprehensive soil classification system of Japan – first approximation. Jpn Agric Res Q 49:217–226. https://doi.org/10.6090/jarq.49.217
Prévost-Bouré NC, Dequiedt S, Thioulouse J, Lelièvre M, Saby NPA, Jolivet C, Arrouays D, Plassart P, Lemanceau P, Ranjard L (2014) Similar processes but different environmental filters for soil bacterial and fungal community composition turnover on a broad spatial scale. PLoS ONE 9:e111667. https://doi.org/10.1371/journal.pone.0111667
Rasche F, Velvis H, Zachow C, Berg G, van Elsas JD, Sessitsch A (2006) Impact of transgenic potatoes expressing anti-bacterial agents on bacterial endophytes is comparable with the effects of plant genotype, soil type and pathogen infection. J Appl Ecol 43:3. https://doi.org/10.1111/j.1365-2664.2006.01169.x
Rodríguez C, Antonielli L, Mitter B, Trognitz F, Sessitsch A (2020) Heritability and functional importance of the Setaria viridis bacterial seed microbiome. Phytobiomes J 4:40–52. https://doi.org/10.1094/PBIOMES-04-19-0023-R
Rui J, Li J, Wang S, An J, Liu W, Lin Q, Yang Y, He Z, Li X (2015) Responses of bacterial communities to simulated climate changes in alpine meadow soil of the Qinghai-Tibet plateau. Appl Environ Microbiol 81:6070–6077. https://doi.org/10.1128/AEM.00557-15
Sahu KP, Kumar A, Sakthivel K, Reddy B, Kumar M, Patel A, Sheoran N, Gopalakrishnan S, Prakash G, Rathour R, Gautam RK (2022) Deciphering core phyllomicrobiome assemblage on rice genotypes grown in contrasting agroclimatic zones: implications for phyllomicrobiome engineering against blast disease. Environ Microbiol 17:28. https://doi.org/10.1186/s40793-022-00421-5
Samuel SO, Suzuki K, Asiloglu R, Harada N (2022) Soil-root interface influences the assembly of the endophytic bacterial community in rice plants. Biol Fertil Soils 58:35–48. https://doi.org/10.1007/s00374-021-01611-y
Shen C, Xiong J, Zhang H, Feng Y, Lin X, Li X, Liang W, Chu H (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211. https://doi.org/10.1016/j.soilbio.2012.07.013
Terrat S, Horrigue W, Dequietd S, Saby NPA, Lelièvre M, Nowak V, Tripied J, Régnier T, Jolivet C, Arrouays D, Wincker P, Cruaud C, Karimi B, Bispo A, Maron PA, Prévost-Bouré NC, Ranjard L (2017) Mapping and predictive variations of soil bacterial richness across France. PLoS ONE 17:e0268101. https://doi.org/10.1371/journal.pone.0186766
Truog E (1930) The determination of the readily available phosphorus of soils. Agron J 22:874–882. https://doi.org/10.2134/agronj1930.00021962002200100008x
van Overbeek L, van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296. https://doi.org/10.1111/j.1574-6941.2008.00469.x
Vendan RT, Yu YJ, Lee SH, Rhee YH (2010) Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J Microbiol 48:559–565. https://doi.org/10.1007/s12275-010-0082-1
Vieira S, Sikorski J, Gebala A, Boeddinghaus RS, Marhan S, Rennert T, Kandeler E, Overmann J (2020) Bacterial colonization of minerals in grassland soils is selective and highly dynamic. Environ Microbiol 22:917–933. https://doi.org/10.1111/1462-2920.14751
Wang M, Sha C, Wu J, Li P, Tan J, Huang S (2022) Comparison of bacterial community in paddy soil after short-term application of pig manure, and the corresponding organic fertilizer. Land 11:9. https://doi.org/10.3390/land11010009
Walitang DI, Kim CG, Kim K, Kang Y, Kim YK, Sa T (2018) The influence of host genotype and salt stress on the seed endophytic community of salt-sensitive and salt-tolerant rice cultivars. BMC Plant Biol 18:51. https://doi.org/10.1186/s12870-018-1261-1
Xu Y, Ge Y, Song J, Rensing C (2020) Assembly of root-associated microbial community of typical rice cultivars in different soil types. Biol Fertil Soils 56:249–260. https://doi.org/10.1007/s00374-019-01406-2
Yu Z, Liang K, Huang G, Wang X, Lin M, Chen Y, Zhou Z (2021) Soil bacterial community shifts are driven by soil nutrient availability along a teak plantation chronosequence in tropical forests in China. Biology (basel) 10:1329. https://doi.org/10.3390/biology10121329
Yuan Y, Si G, Wang J, Luo T, Zhang G (2014) Bacterial community in alpine grasslands along an altitudinal gradient on the Tibetan Plateau. FEMS Microbiol Ecol 87:121–132. https://doi.org/10.1111/1574-6941.12197
Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S, van der Lelie D, Gilbert JA (2015) The soil microbiome influences grapevine-associated microbiota. Mbio 6:e02527-e2614. https://doi.org/10.1128/mBio.02527-14
Zhang X, Ma YN, Wang X, Liao K, He S, Zhao X, Guo H, Zhao D, Wei HL (2022) Dynamics of rice microbiomes reveal core vertically transmitted seed endophytes. Microbiome 10:216. https://doi.org/10.1186/s40168-022-01422-9
Zhang X, Zhong Z, Gai X, Du X, Bian F, Yang C, Gao G, Wen X (2019) Changes of root endophytic bacterial community along a chronosequence of intensively managed lei bamboo (Phyllostachys praecox) forests in subtropical China. Microorganisms 7:616. https://doi.org/10.3390/microorganisms7120616
Funding
This work was funded by JSPS KAKENHI Grant Number JP21K14952. The sequencing analysis was the result of using research equipment shared in the MEXT Project for promoting public utilization of advanced research infrastructure (Program for supporting introduction of the new sharing system) at Niigata University, Grant Number JPMXS0421100320.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
This study does not involve animals.
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.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Samuel, S.O., Suzuki, K., Asiloglu, R. et al. Rice endophytic communities are strongly dependent on microbial communities specific to each soil. Biol Fertil Soils 59, 733–746 (2023). https://doi.org/10.1007/s00374-023-01743-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-023-01743-3