This study investigated the diversity, structure and nutrient pathways of the root-associated bacterial endophytes of maize plant cultivated using different fertilizers to verify the claim that inorganic fertilizers have some toxic effects on plant microbiome and not are ecofriendly. Whole DNA was extracted from the roots of maize plants cultivated with organic fertilizer, inorganic fertilizer and maize planted without any fertilizer at different planting sites in an experimental field and sequenced using shotgun metagenomics. Our results using the Subsystem database revealed a total of 28 phyla and different nutrient pathways in all the samples. The major phyla observed were Firmicutes, Bacteroidetes, Actinobacteria, Proteobacteria, Acidobacteria, Chloroflexi, Verrucomicrobia, Tenericutes, Planctomycetes, Cyanobacteria, and Chlorobi. Bacteroidetes dominated maize from organic fertilizer sites, Firmicutes dominated the no fertilizers site while Proteobacteria dominated Inorganic fertilizer. The diversity analysis showed that the abundance of endophytic bacteria in all the sites is in the order organic fertilizer (FK) > no fertilizer (CK) > inorganic fertilizer (NK). Furthermore, the major nutrient cycling pathways identified are linked with nitrogen and phosphorus metabolism which were higher in FK samples. Going by the results obtained, this study suggests that organic fertilizer could be a boost to sustainable agricultural practices and should be encouraged. Also, a lot of novel endophytic bacteria groups were identified in maize. Mapping out strategies to isolate and purify this novel endophytic bacteria could help in promoting sustainable agriculture alongside biotechnological applications in future.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Sequence data obtained in this work have been deposited in the NCBI Sequence Read Archive under Accession Number PRJNA607664.
Acevedo E, Galindo-Castañeda T, Prada F, Navia M, Romero HM (2014) Phosphate-solubilizing microorganisms associated with the rhizosphere of oil palm (Elaeis guineensis Jacq.) in Colombia. Appl Soil Ecol 80:26–33
Ahmad F, Ahmad I, Khan M (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163(2):173–181
Akinsanya MA, Goh JK, Lim SP, Ting ASY (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genom Data 6:159–163
Alori ET, Babalola OO, Prigent-Combaret C (2019) Impacts of microbial inoculants on the growth and yield of maize plant. Open Agric J 13(1):1–8
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
Bulgari D, Casati P, Crepaldi P, Daffonchio D, Quaglino F, Brusetti L, Bianco PA (2011) Restructuring of endophytic bacterial communities in grapevine yellows-diseased and recovered Vitis vinifera L. plants. Appl Environ Microbiol 77(14):5018–5022
Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108(34):14288–14293
Campisano A, Antonielli L, Pancher M, Yousaf S, Pindo M, Pertot I (2014) Bacterial endophytic communities in the grapevine depend on pest management. PLoS ONE 9(11):e112763
Carrell AA, Frank C (2015) Bacterial endophyte communities in the foliage of coast redwood and giant sequoia. Front Microbiol 6:1008
Celador-Lera L, Menéndez E, Flores-Félix JD, Mateos PF, Rivas R (2016) Analysis of the PGPB potential of bacterial endophytes associated with maize. In: González-Andrés F, James E (eds) Biological nitrogen fixation and beneficial plant-microbe interaction. Springer, Cham, pp 23–35
Chung EJ, Park TS, Jeon CO, Chung YR (2012) Chitinophaga oryziterrae sp. Nov., isolated from the rhizosphere soil of rice (Oryza sativa L.). Int J Syst Evol Microbiol 62(12):3030–3035
Correa-Galeote D, Bedmar EJ, Arone GJ (2018) Maize endophytic bacterial diversity as affected by soil cultivation history. Front Microbiol 9:484
Correa-Galeote D, Bedmar EJ, Fernández-González AJ, Fernández-López M, Arone GJ (2016) Bacterial communities in the rhizosphere of amilaceous maize (Zea mays L.) as assessed by pyrosequencing. Front Microbiol 7:1016
Das A, Varma A (2009) Symbiosis: the art of living. In: Symbiotic fungi. Springer, pp 1–28
De Tender C (2017) Microbial community analysis in soil (rhizosphere) and the marine (plastisphere) environment in function of plant health and biofilm formation. Doctor (Ph.D.) in biotechnology Thesis, Ghent University, pp 1–274.
Ding T, Palmer MW, Melcher U (2013) Community terminal restriction fragment length polymorphisms reveal insights into the diversity and dynamics of leaf endophytic bacteria. BMC Microbiol 13(1):1
Du-Plessis J (2003) Maize production. Department of Agriculture, Pretoria, pp 1–38
Dudeja SS, Giri R, Saini R, Suneja-Madan P, Kothe E (2012) Interaction of endophytic microbes with legumes. J Basic Microbiol 52(3):248–260. https://doi.org/10.1002/jobm.201100063
Esmaeel Q, Pupin M, Kieu NP, Chataigné G, Béchet M, Deravel J, Krier F, Höfte M, Jacques P, Leclère V (2016) Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. Microbiol. Open 5(3):512–526
Fadiji AE, Babalola OO (2020a) Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front Bioeng Biotechnol 8:467
Fadiji AE, Babalola OO (2020b) Metagenomics methods for the study of plant-associated microbial communities: a review. J Microbiol Methods 170:105860
Fouda AH, Hassan SE-D, Eid AM, Ewais EE-D (2015) Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss.). Ann Agric Sci 60(1):95–104
Griffin EA, Carson WP (2018) Tree endophytes: cryptic drivers of tropical forest diversity. In: Pirttilä A, Frank A (eds) Endophytes of forest trees. Forestry sciences, vol 86. Springer, Cham, pp 63–103
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79(3):293–320
Hong CE, Kim JU, Lee JW, Bang KH, Jo IH (2019) Metagenomic analysis of bacterial endophyte community structure and functions in Panax ginseng at different ages. 3 Biotech 9(8):300
Ikenaga M, Tabuchi M, Kawauchi T, Sakai M (2016) Application of locked nucleic acid (LNA) primer and PCR clamping by LNA oligonucleotide to enhance the amplification of internal transcribed spacer (ITS) regions in investigating the community structures of plant-associated fungi. Microbes Environ 31(3):339–348. https://doi.org/10.1264/jsme2.ME16085
Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12(4):656–664
Khomtchouk BB, Hennessy JR, Wahlestedt C (2017) shinyheatmap: ultra fast low memory heatmap web interface for big data genomics. PLoS ONE 12(5):e0176334
Kniss AR, Savage SD, Jabbour R (2016) Commercial crop yields reveal strengths and weaknesses for organic agriculture in the United States. PLoS ONE 11(8):e0165851
Kumar M, Saxena R, Tomar RS (2017) Endophytic microorganisms: promising candidate as biofertilizer. In: Panpatte D, Jhala Y, Vyas R, Shelat H (eds) Microorganisms for green revolution. Microorganisms for sustainability, vol 6. Springer, Singapore, pp 77–85
Li H-Y, Wei D-Q, Shen M, Zhou Z-P (2012) Endophytes and their role in phytoremediation. Fungal Divers 54(1):11–18
Lin W, Lin M, Zhou H, Wu H, Li Z, Lin W (2019) The effects of chemical and organic fertilizer usage on rhizosphere soil in tea orchards. PLoS ONE 14(5):e0217018
Liu Y, Wang R, Li Y, Cao Y, Chen C, Qiu C, Bai F, Xu T, Zhang X, Dai W (2017) High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of “Beijing” hybrid maize planted in China. Plant Growth Regul 81(2):317–324
Marag PS, Suman A, Gond S (2018) Prospecting endophytic bacterial colonization and their potential plant growth promoting attributes in hybrid maize (Zea mays L.). Int J Curr Microbiol Appl Sci 7:1292–1304
Mashiane AR, Adeleke RA, Bezuidenhout CC, Chirima GJ (2018) Community composition and functions of endophytic bacteria of Bt maize. S Afri J Sci 114(7–8):88–97
Menéndez E et al (2016) Analysis of cultivable endophytic bacteria in roots of maize in a soil from León province in Mainland Spain. In: González-Andrés F, James E (eds) Biological nitrogen fixation and beneficial plant–microbe interaction. Springer, Cham, pp 45–53
Midekssa M, Loscher C, Schmitz R, Assefa F (2015) Characterization of phosphate solubilizing rhizobacteria isolated from lentil growing areas of Ethiopia. Afr J Microbiol Res 9(25):1637–1648
Nkoa R (2014) Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review. Agron Sustain Dev 34(2):473–492
Omomowo OI, Babalola OO (2019) Bacterial and fungal endophytes: tiny giants with immense beneficial potential for plant growth and sustainable agricultural productivity. Microorganisms 7(11):481
Ormskirk MM, Narciso J, Hampton JG, Glare TR (2019) Endophytic ability of the insecticidal bacterium Brevibacillus laterosporus in Brassica. PloS One 14(5):e0216341
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 Ecology 938546:1–10
Phukon M, Sahu P, Srinath R, Nithya A, Babu S (2013) Unusual occurrence of S. taphylococcus warneri as endophyte in fresh fruits along with usual Bacillus spp. J Food Saf 33(1):102–106
Puri RR, Adachi F, Omichi M, Saeki Y, Yamamoto A, Hayashi S, Ali MA, Itoh K (2019) Metagenomic study of endophytic bacterial community of sweet potato (Ipomoea batatas) cultivated in different soil and climatic conditions. World J Microbiol Biotechnol 35(11):176
Puri RR, Dangi SR, Dhungana SA, Itoh K (2018) Diversity and plant growth promoting ability of culturable endophytic bacteria in Nepalese sweet potato. Adv Microbiol 8(9):734–761
Rai R, Dash PK, Prasanna B, Singh A (2007) Endophytic bacterial flora in the stem tissue of a tropical maize (Zea mays L.) genotype: isolation, identification and enumeration. World J Microbiol Biotechnol 23(6):853–858
Reganold JP, Wachter JM (2016) Organic agriculture in the twenty-first century. Nat Plants 2(2):1–8
Sandhya V, Shrivastava M, Ali SZ, Prasad VSSK (2017) Endophytes from maize with plant growth promotion and biocontrol activity under drought stress. Russ Agric Sci 43(1):22–34
Sauvêtre A, Schröder P (2015) Uptake of carbamazepine by rhizomes and endophytic bacteria of Phragmites australis. Front Plant Sci 6:83
Seghers D, Wittebolle L, Top EM, Verstraete W, Siciliano SD (2004) Impact of agricultural practices on the Zea mays L. endophytic community. Appl Environ Microbiol 70(3):1475–1482
Sengupta S, Ganguli S, Singh PK (2017) Metagenome analysis of the root endophytic microbial community of Indian rice (O. sativa L.). Genom Data 12:41–43
Shah N, Tang H, Doak TG, Ye Y (2011) Comparing bacterial communities inferred from 16S rRNA gene sequencing and shotgun metagenomics. In: Biocomputing. World Scientific, pp 165–176
Sharma A, Chetani R (2017) A review on the effect of organic and chemical fertilizers on plants. Int J Res Appl Sci Eng 5(2):677–680
Sivasakthi S, Usharani G, Saranraj P (2014) Biocontrol potentiality of plant growth promoting bacteria (PGPR)-Pseudomonas fluorescens and Bacillus subtilis: a review. Afr J Agric Res 9(16):1265–1277
Srivastava S, Verma PC, Chaudhry V, Singh N, Abhilash P, Kumar KV, Sharma N, Singh N (2013) Influence of inoculation of arsenic-resistant Staphylococcus arlettae on growth and arsenic uptake in Brassica juncea (L.) Czern. Var. R-46. J Hazard Mater 262:1039–1047
Staniek A, Woerdenbag HJ, Kayser O (2008) Endophytes: exploiting biodiversity for the improvement of natural product-based drug discovery. J Plant Interact 3(2):75–93
Sun R, Zhang X-X, Guo X, Wang D, Chu H (2015) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18
Szilagyi-Zecchin VJ, Ikeda AC, Hungria M, Adamoski D, Kava-Cordeiro V, Glienke C, Galli-Terasawa LV (2014) Identification and characterization of endophytic bacteria from corn (Zea mays L.) roots with biotechnological potential in agriculture. AMB Express 4(1):1–9
Tumangger BS, Nadilla F, Baiduri N, Mardina V (2018). In vitro screening of endophytic fungi associated with mangroveas biofertilizer on the growth of black rice (Oryza sativa L." Cempo Ireng"). In: IOP conference series: materials science and engineering, vol 420(1), p 012080
U. S. Department of Agriculture [USDA] (2014) Organic regulations. Title 7, subtitle B, chapter I, subchapter M, section 205. https://www.ams.usda.gov/AMSv1.0/NOPOrganicStandards
Van Bruggen A, Finckh M (2016) Plant diseases and management approaches in organic farming systems. Annu Rev Phytopathol 54:25–54
Vejan P, Abdullah R, Khadiran T, Ismail S, Boyce N (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21(5):573
Vincent JM (1970) A manual for the practical study of the root-nodule bacteria. Wiley, Hoboken, p 440
Wezel A, Bellon S, Doré T, Francis C, Vallod D, David C (2009) Agroecology as a science, a movement and a practice. A review Agron Sustain Dev 29(4):503–515
Wilke A, Harrison T, Wilkening J, Field D, Glass EM, Kyrpides N, Mavrommatis K, Meyer F (2012) The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinform 13(1):141
Xia Y, Sahib MR, Amna A, Opiyo SO, Zhao Z, Gao YG (2019) Culturable endophytic fungal communities associated with plants in organic and conventional farming systems and their effects on plant growth. Sci Rep 9(1):1669
Xia Y, DeBolt S, Dreyer J, Scott D, Williams MA (2015) Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Front Plant Sci 6:490
Yan X, Gong W (2010) The role of chemical and organic fertilizers on yield, yield variability and carbon sequestration—results of a 19-year experiment. Plant Soil 331(1–2):471–480
Yang R, Liu P, Ye W (2017) Illumina-based analysis of endophytic bacterial diversity of tree peony (Paeonia Sect. Moutan) roots and leaves. Braz J Microbiol 48(4):695–705
Yu S, Teng C, Bai X, Liang J, Song T, Dong L, Jin Y, Qu J (2017) Optimization of siderophore production by bacillus sp PZ-1 and its potential enhancement of phytoextration of Pb from soil. J Microbiol Biotechnol 27(8):1500–1512
Zhu Z, Chen D (2002) Nitrogen fertilizer use in China-Contributions to food production, impacts on the environment and best management strategies. Nutr Cycl Agroecosys 63(2–3):117–127
AEF appreciates National Research Foundation, South Africa/The World Academy of Science African Renaissance (Ref: UID116107) for the stipend which was of great help in his Ph.D. studies. ASA appreciates North-West University for a postdoctoral fellowship award. OOB appreciates the National Research Foundation, South Africa for the research Grant (UID123634) that supported research in her laboratory.
The study was funded by the National Research Foundation, South Africa (UID123634).
Conflict of interest
The author declares that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Fadiji, A.E., Ayangbenro, A.S. & Babalola, O.O. Metagenomic profiling of the community structure, diversity, and nutrient pathways of bacterial endophytes in maize plant. Antonie van Leeuwenhoek 113, 1559–1571 (2020). https://doi.org/10.1007/s10482-020-01463-w
- Endophytic microbes
- Fertilizer application
- Plant associated microbes
- Shotgun metagenomics
- Zea mays