Abstract
Coffea arabica L. and Coffea canephora L. are coffee species most consumed and marketed in the world. The coffee crop requires a large amount of nitrogen, which shows the importance of knowledge of the population of nitrogen-fixing bacteria (NFB) from the rhizosphere of these crops. These microorganisms may help the reduction of nitrogen fertilizing. However, there is no production of NFB inoculum in the coffee. Therefore, our objective was to evaluate the diversity of potential nitrogen-fixing bacteria (PNFB) in the rhizosphere of C. arabica and C. canephora. The microbial DNA of the soil was extracted, amplified through PCR, and sequenced at the Illumina Miseq. platform. The PNFB prediction was performed using the program PICRUSt2. Three hundred and thirty-seven amplicon sequence variants (ASVs) were identified as PNFB in two coffee species. Xanthobacteraceae, Rhizobium multhospitiium, Rhizobium mesosinicum, and Bradyrhizobium sp. were detected in all samples and main components of the core microbiota of the coffee plant rhizosphere. Some ASVs are exclusive from one of the coffee farms, showing that the coffee specie cultivated may influence the PNFB communities. However, edaphoclimatic factors and soil chemical attributes can also influence the distribution of ASVs in coffee soil. In the C. canephora, the PNFB diversity was influenced by the altitude and the soil chemical attributes, while the altitude and the phosphorus content influenced the PNFB population in C. arabica. Our results are important to the understanding of the PNFB dynamic in coffee soil and for the agricultural inputs bioprospecting to coffee.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The authors declare the data availability from the article for interested persons. All authors authorized the submission and publication of the paper.
References
Adachi K, Nakatani M, Mochida H (2002) Isolation of an endophytic diazotroph, Klebsiella oxytoca, from sweet potato stems in japan. Soil Sci Plant Nutr 48(6):889–895. https://doi.org/10.1080/00380768.2002.10408717
Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveals that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512. https://doi.org/10.1074/jbc.M112.433300
Baldani JI, Baldani VLD (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Ciênc 77(3):549–579. https://doi.org/10.1590/S0001-37652005000300014
Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Cabresa-Rodriguíz A, Trejo-Calzada R, Peña CG, Arreola-Ávilla JG, Nava-Reyna E, Vaca-Paniagua F, Díaz-Velásquez C, Meza-Herrera C (2020) A metagenomic approach in the evaluation of the soil microbiome in coffee plantations under organic and conventional production in tropical agroecosystems. Emir J Food Agric 32:263–270. https://doi.org/10.9755/ejfa.2020.v32.i4.2092
Caldwell AC, Silva LCF, da Silva CC, Ouverney CC (2015) Prokaryotic diversity in the rhizosphere of organic, intensive, and transitional coffee farms in Brazil. PLoS ONE 10:e0106355. https://doi.org/10.1371/journal.pone.0106355
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJÁ, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 7:581–583. https://doi.org/10.1038/nmeth.3869
Cassamo CT, Mangueze AVJ, Leitão AE, Paes IP, Moreira R, Campa C, Chiulele R, Reis FO, Marques I, Scotti-Campos P, Lidon FC, Partelli FL, Ribeiro-Barros AI, Ramalho JC (2022) Shade and altitude implications on the physical, chemical attributes of green coffee beans from Gorongosa Mountain. Mozambique Agron 12(10):2540. https://doi.org/10.3390/agronomy12102540
CEPEA-ESALQ/USP (2022) GDP of Brazilian Agribusiness - Center for Advanced Studies in Applied Economics (in Portuguese). CEPEA-Esalq/USP. https://www.cepea.esalq.usp.br/br/pib-do-agronegocio-brasileiro.aspx
Chaudhari D, Rangappa K, Das A, Layek J, Basavaraj S, Kandpal BK, Shouche Y, Rahi P (2020) Pea (Pisum sativum L.) plant shapes its rhizosphere microbiome for nutrient uptake and stress amelioration in acidic soils of the north-east region of India. Front Microbiol 11:1–15. https://doi.org/10.3389/fmicb.2020.00968
Curi MA, Jiménez VH, Ibarra JPJ (2019) Native bacterial strains with plant growth promotion activities isolated from Coffea spp. rhizosphere in Pichanaqui, Perú. Biotecnol Vegetal 19:285–295
De Sousa LP, Guerreiro-Filho O, Mondego JMC (2022) The rhizosphere microbiomes of five species of coffee trees. Microbiol Spectr 10:e00444. https://doi.org/10.1128/spectrum.00444-22
Defelipo BV, Ribeiro AC (1997) Soil chemical analysis (methodology) [In Portuguese]. Bol Extensão Universidade Federal De Viçosa 28:1–26
Döbereiner J (1997) Biological nitrogen fixation in the tropics: social and economic contributions. Soil Biol Biochem 29:771–774. https://doi.org/10.1016/S0038-0717(96)00226-X
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MG (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. https://doi.org/10.1038/s41587-020-0548-6
Elo S, Suominen I, Kämpfer P, Juhanoja J, Salkinoja-Salonen M, Haahtela K (2001) Paenobacillus borealis sp. nov., a nitrogen- fixing species isolated from spruce forest humus in Finland. Int J Syst Evol Microbiol 51:535–545. https://doi.org/10.1099/00207713-51-2-535
Fox A, Lüscher A, Widmer F (2020) Plant species identity drives soil microbial community structures that persist under a following crop. Ecol Evol 10:8652–8668. https://doi.org/10.1002/ece3.6560
Gao H, Li S, Wu F (2021) Impact of Intercropping on the Diazotrophic Community in the soils of continuous cucumber cropping systems. Front Microbiol 12:1–13. https://doi.org/10.3389/fmicb.2021.630302
Grossman JM, Sheaffer C, Wyse D, Graham PH (2005) Characterization of slow-growing root nodule bacteria from Inga oerstediana in organic coffee agroecosystems in Chiapas, Mexico. Appl Soil Ecol 29:236–251. https://doi.org/10.1016/j.apsoil.2004.12.008
Incaper (2023) Coffee growing (in Portuguese). https://incaper.es.gov.br/cafeicultura#:~:text=O%20Esp%C3%ADrito%20Santo%20%C3%A9%20o,Bruto%20(PIB)%20Agr%C3%ADcola%20capixaba)
International Coffee Organization (2022) Historical data on the global coffee trade. https://www.ico.org/new_historical.asp
Kamilova F, Kravchenko LV, Shaposhnikov AI, Makarova TAN, Lugtenberg B (2006) Organic acids, sugars, and l- tryptophane in exudates of vegetable growing on stonewool and their effects of rhizosphere bacteria. Mol Plant Microbe Interact 19:250–256. https://doi.org/10.1094/MPMI-19-0250
Köberl M, Erlacher A, Ramadan EM, El-Arabi TF, Müller H, Bragina A, Berg G (2016) Comparisons of diazotrophic communities in native and agricultural desert ecosystems reveal plants as important drivers in diversity. FEMS Microbiol Ecol 92:1–11. https://doi.org/10.1093/femsec/fiv166
Kour D, Rana KL, Yadav NA, Yadav N, Kumar M, Kumar V, Vyas P, Dhaliwal H, Saxena A (2020) Microbial biofertilizers: bioresources and eco-friendly tecnologies for agricultural and environmental and sustainability. Biocatal Agric Biotechnol 23:101487. https://doi.org/10.1016/j.bcab.2019.101487
LahtI L, Shetty S (2017) Tools for microbiome analysis in R. Microbiome package version 1.7.21. R/Bioconductor. http://microbiome.github.com/microbiome
Lindström K, Mousavi SA (2019) Effectiveness of nitrogen fixation in rhizobia. Microb Biotechnol 13:1314–1335. https://doi.org/10.1111/1751-7915.13517
Liu Z, Li Q, Li Y, Guan G, Chen S (2019) Paenibacillus strains with nitrogen fixation and multiple beneficial properties for promoting plant growth. PeerJ 7:e7445. https://doi.org/10.7717/peerj.7445
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet.journal 17:10. https://doi.org/10.14806/ej.17.1.200
Morvan S, Meglouli H, Sahraoui ALH, Hijri M (2020) Into the wild blueberry (Vaccinium angustifolium) rhizosphere microbiota. Environ Microbiol 22:3803–3822. https://doi.org/10.1111/1462-2920.15151
Naqqash T, Imram A, Hameed S, Majeed A, Iqbal J, Hanif MK, Ejaz S, Malik KA (2020) First report of diazotrophic Brevundimonas spp. as growth enhancer and root colonizer of potato. Sci Rep 10:12893. https://doi.org/10.1038/s41598-020-69782-6
Pereira LL, Moreira TR (2021) Quality determinants. In: Coffee production. Food Engineering Series. (eBook). Springer Nature Switzerland AG. https://doi.org/10.1007/978-3-030-54437
Prosser J, Head I, Stein L (2014) The family nitrosomonadaceae. In: Rosenberg E, DeLong EF, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, pp 901–918. https://doi.org/10.1007/978-3-642-30197-1_372
Rascio N, La Rocca N (2013) Biological nitrogen fixation. In: Fath B (ed) Encyclopedia of ecology, vol 2. Elsevier, Amsterdam, pp 264–279
Reis Junior FB, et al (2011) Biological nitrogen fixation: a revolution in agriculture (in Portuguese). In: Faleiro FG, Andrade SEM, Reis Junior FB (eds) Biotechnology—state of the art and applications in agriculture. 1. Embrapa Cerrados ed., Planaltina, p 730
Siles JA, Cajthaml T, Minerbi S, Margesin R (2016) Effect of altitude and season on microbial activity, abundance and community structure in Alpine Forest soils. FEMS Microbiol Ecol 92:1–12. https://doi.org/10.1093/femsec/fiw008
Siles JA, Margesin R (2016) Abundace and diversity of bacterial, archaeal, and fungal communities along na altitudinal gradient in alpine forest soils: what are the driving factors? Microb Ecol 72(1):207–220. https://doi.org/10.1007/s00248-016-0748-2
Silva MCS, Veloso TGR, Borchardt VB, Pereira LL, Anastácio LM, Kasuya MCN (2020) Diversity of nitrogen-fixing bacteria in coffee crops (Coffea arabica L.). Rev Ifes Ciênc 6:12–21. https://doi.org/10.36524/ric.v6i3.852
Suharjono S, Yuliatin E (2022) Bacteria communities of coffee plant rhizosphere and their potency as plant growth promoting. Biodiversitas 23:5822–5834. https://doi.org/10.13057/biodiv/d231136
Taques RC, Dadalto GG (2007) Agroclimatological zoning for the conilon coffee culture in the state of Espírito Santo (in Portuguese). In: Ferrão RG, Fonseca AFA, Bragança SM, Ferrão MAG, De Muner LH (eds) Conilon coffee. Incaper Vitória, pp 50–63
Tran DM (2022) Rhizosphere microbiome dataset of Robusta coffee (Coffea canephora L.) grown in the Central Highlands, Vietnam, based on 16S rRNA metagenomics analysis. Data Br 42:108106. https://doi.org/10.1016/j.dib.2022.108106
Upadhyay SK, Srivastava AK, Rajput VD, Chauhan PK, Bhojiya AA, Jain D, Chaubey G, Dwivedi P, Sharma B, Minkina T (2022) Root exudates: mechanistic insight of plant growth promoting rhizobacteria for sustainable crop production. Front Microbiol 13:916488. https://doi.org/10.3389/fmicb.2022.916488
Urgiles-Gómez N, Avila-Salem ME, Loján P, Encalada M, Hurtado L, Araujo S, Collahuazo Y, Guachanamá J, Poma N, Granda K, Robles A, Senés C, Cornejo P (2021) Plant growth-promoting microorganisms in coffee production: from isolation to field application. Agronomy 11:1531. https://doi.org/10.3390/agronomy11081531
Veloso TGR, da Silva MCS, Cardoso WS, Guarçoni RC, Kasuya MCM, Pereira LL (2020) Effects of environmental factors on microbiota of fruits and soil of Coffea arabica in Brazil. Sci Rep 10:14692. https://doi.org/10.1038/s41598-020-71309-y
Videira SS, Oliveira DM, Morais RF, Borges WL, Baldani VLD, Baldani JI (2012) Genetic diversity and plant growth promoting traits of diazotrophic bacteria isolated from two Pennisetum purpureum Schum. genotypes grown in the field. Plant Soil 356(1–2):51–66. https://doi.org/10.1007/s11104-011-1082-6
Xue B, Yu J, Zhang J (2022) Microbial diversity analysis of Vineyard son the Eastern foothills of the Helan Mountain region using high-throughput sequencing. Food Sci Technol (Campinas) 42:2022. https://doi.org/10.1590/fst.66320
Zhang X, Tong J, Dong M, Aktar K, He B (2022) Isolation, identification and characterization of nitrogen fixing endophytic bacteria and their effects on cassava production. PeerJ 10:e12677. https://doi.org/10.7717/peerj.12677.eCollection. (eCollection 2022)
Zhu W, Huang J, Li M, Wang G (2015) Genomic analysis of Skermanella stibiiresistens types strain SB22T. Stand Genomic Sci 9(3):1211–1220. https://doi.org/10.4056/sigs.5751047
Acknowledgements
The authors would like to thank the Sul Serrana of Espírito Santo Free Admission Credit Cooperative—Sicoob (23186000886201801), the Coordination of Superior Level Staff Improvement—CAPES, the National Council for Scientific and Technological Development (CNPq), the IFES for supporting the research (PRPPG n°. 12/2021), Incaper, Embrapa, Fapemig, and Fapes.
Author information
Authors and Affiliations
Contributions
Conceptualization, validation, investigation, writing, formal analysis: VBB, KMSM, TGRV, JMRL, LLP, and MCSS. Data processing and analysis: KMSM, TGRV, JMRL, LLP, and MCSS. The investigation, writing—review and editing: VBB, KMSM, TGRV, JMRL, LFC, LLP, and MCSS.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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
Bullergahn, V.B., Menezes, K.M.S., Veloso, T.G.R. et al. Diversity of potential nitrogen-fixing bacteria from rhizosphere of the Coffea arabica L. and Coffea canephora L.. 3 Biotech 14, 27 (2024). https://doi.org/10.1007/s13205-023-03875-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-023-03875-7