Enhanced mycorrhiza helper bacterial inoculant for improving the health of Arabica coffee seedlings grown in nematode-infected soil

##plugins.themes.bootstrap3.article.main##

REGINAWANTI HINDERSAH
https://orcid.org/0000-0003-0281-2363
IIS NUR ASYIAH
WIDI AMARIA
BETTY NATALIE FITRIATIN
https://orcid.org/0000-0002-3749-5081
IMAM MUDAKIR
SAON BANERJEE
https://orcid.org/0000-0001-8213-1036

Abstract

Abstract. Hindersah R, Asyiah IN, Amaria W, Fitriatin BN, Mudakir I, Banerjee S. 2025. Enhanced mycorrhiza helper bacterial inoculant for improving the health of Arabica coffee seedlings grown in nematode-infected soil. Biodiversitas 26: 127-124. The Arbuscular Mycorrhizal Fungi (AMF) and Mycorrhiza Helper Bacteria (MHB) combine to combat the Pratylenchus coffeae nematode infection on coffee plantations sustainably and synergistically. Additionally, AMF facilitates the availability of phosphorus in plants. The objectives of present study are to formulate an enhanced MHB liquid inoculant containing Bacillus subtilis and Pseudomonas diminuta, and to test its efficacy in controlling P. coffeae in roots, improving P status in soil and plants, and promoting the growth of Arabica coffee seedlings infested with the nematodes. MHB liquid inoculant was enhanced by optimizing molasses, nitrogen, phosphorus, and MHB concentrations. The five treatments were used, and five replications were in a randomized block-design greenhouse experiment to investigate the AMF Glomus agregatum and MHB inoculant. The improved substrate for MHB liquid inoculant comprised 2% molasses, 0.05% NH4Cl, and 0.1% KH2PO4, with a 2:3 initial volume ratio of B. subtilis and P. diminuta. Scaling up the MHB inoculant in the 2 L reactor boosted the bacterial population to 1010 CFU/mL and the P content to 100 mg/kg. Applying 200 AMF spores and 109 CFU/mL MHB increased leaf number, plant P uptake, and soil P while decreasing root damage and nematode population in soil and roots. Combined AMF and MHB reduced P. coffeae infestation in roots by 70.79% and increased P content in soil and plants by 57.2% and 61.9%, respectively.

##plugins.themes.bootstrap3.article.details##

References
Andriani Y, Safitri R, Rochima E, Fakhrudin SD. 2017. Characterization of Bacillus subtilis and B. licheniformis potentials as probiotic bacteria in Vanamei shrimp feed (Litopenaeus vannamei Boone, 1931). Nusantara Biosci 9: 188-193. DOI: 10.13057/nusbiosci/n090214.
Asyiah IN., Wiryadiputra S., Fauzi I., Harni R. 2015. Population of pratylenchus coffeae (Z) and growth of arabica coffee seedling inoculated by Pseudomonas diminuta and Bacillus subtilis. Pelita Perkebunan 31 (1): 30-40.
Asyiah IN, Hindersah R, Harni R, Fitriatin BN, Anggraeni W. 2021. Mycorrhizal fungi Glomus spp. propagation in zeolite enriched with mycorrhiza helper bacteria for controlling nematode in coffee. IOP Conf Ser: Earth Environ Sci 883: 012021. DOI: 10.1088/1755-1315/883/1/012021.
Ayalew B, Hylander K, Adugna G, Zewdie B, Zignol F, Tack AJM. 2024. Impact of climate and management on coffee berry disease and yield in coffee’s native range. Basic Appl Ecol 76: 25-34. DOI: 10.1016/j.baae.2024.01.006.
BPS [Badan Pusat Statistik]. 2023. Indonesian Coffee Statstics 2022. BPS, Jakarta. https://www.bps.go.id/en/publication/2023/11/30/abde293e6c 0fc5d45aaa9fe8/indonesian-coffee-statistics-2022.html. [Indonesian]
Banerjee S, Mukherjee A, Sattar A, Biswas B. 2016. Change detection of annual temperature and rainfall in Kalimpong station under hill zone of West Bengal. Indian J Hill Farm 28 (2): 81-84.
Barbosa P, Faria JMS, Cavaco T, Figueiredo AC, Mota M, Vicente CSL. 2024. Nematicidal activity of phytochemicals against the root-lesion nematode Pratylenchus penetrans. Plants 13 (5): 726. DOI: 10.3390/plants13050726.
Beroya-Eitner MA. 2016. Ecological vulnerability indicators. Ecol Indic 60: 329-334. DOI: 10.1016/j.ecolind.2015.07.001.
Bhavya K, Subhash Reddy R, Triveni S. 2017. Comparitive study on quality parameters and viability of carrier and liquid biofertilizers. Intl J Pure Appl Biosci 5 (4): 1702-1709. DOI: 10.18782/2320-7051.5706.
Brundrett MC. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320: 37-77. DOI: 10.1007/s11104-008-9877-9.
Bunn C, Läderach P, Jimenez JGP, Montagnon C, Schilling T. 2015. Multiclass classification of agro-ecological zones for Arabica coffee: An improved understanding of the impacts of climate change. PLoS One 10 (10): e0140490. DOI: 10.1371/journal.pone.0140490.
Cepeda-Siller M, Cerna-Cha?vez E, Ochoa-Fuentes YM, Medina MDD, Cruz FG, Jua?rez AH. 2018. Biological effectiveness of the nematicide Nemmax on coffee (Coffea arabica L.). Rev Mex Cienc Agric 9 (2): 459-464. DOI: 10.29312/remexca.v9i2.1085.
de Andrade LA, Santos CHB, Frezarin ET, Sales LR, Rigobelo EC. 2023. Plant growth-promoting rhizobacteria for sustainable agricultural production. Microorganisms 11 (4): 1088. DOI: 10.3390/microorganisms11041088.
de Beenhouwer M, Muleta D, Peeters B, Van Geel M, Lievens B, Honnay O. 2015. DNA pyrosequencing evidence for large diversity differences between natural and managed coffee mycorrhizal fungal communities. Agron Sustain Dev 35: 241-249. DOI: 10.1007/s13593-014-0231-8.
Dias CG, Martins FB, Martins MA. 2024. Climate risks and vulnerabilities of the Arabica coffee in Brazil under current and future climates considering new CMIP6 models. Sci Total Environ 907: 167753. DOI: 10.1016/j.scitotenv.2023.167753.
Enemuor S. 2014. Isolation, characterization and biodegradation assay of glyphosate utilizing bacteria from exposed rice farm. Intl J Sci Eng Res 5 (2): 1672-1700.
Fitriatin BN, Budiman MN, Suryatmana P, Kamaluddin NN, Ruswandi D. 2023. Phosphate availability, P-uptake, phosphatase, and yield of maize (Zea mays L.) affected by kaolin-based P-solubilizer and P fertilizer in Inceptisols. Jurnal Kultivasi 22 (1): 71-76. DOI: 10.24198/kultivasi.v22i1.42847.
Ghini R, Hamada E, Pedro Júnior MJ, Marengo JA, do Valle Gonçalves RR. 2008. Risk analysis of climate change on coffee nematodes and leaf miner in Brazil. Pesq Agropec Bras 43 (2): 187-194. DOI: 10.1590/S0100-204X2008000200005.
Gough EC, Owen KJ, Zwart RS, Thompson JP. 2020. A systematic review of the effects of arbuscular mycorrhizal fungi on root-lesion nematodes. Front Pl Sci 11: 923. DOI: 10.3389/fpls.2020.00923.
Guarnizo ÁL, Navarro-Ródenas A, Calvo-Polanco M, Marqués-Gálvez JE, Morte A. 2023. A mycorrhizal helper bacterium alleviates drought stress in mycorrhizal Helianthemum almeriense plants by regulating water relations and plant hormones. Environ Exp Bot 207: 105228. DOI: 10.1016/j.envexpbot.2023.105228.
Hindersah R, Asyiah IN, Harni R, Rahayu DS, Fitriatin BF. 2022b. Formulation of soil beneficial microbes solid inoculant for controlling nematode in coffee. Jurnal Penelitian Pertanian Terapan 22 (1): 58-66. DOI: 10.25181/jppt.v22i1.2126.
Hindersah R, Lilipaly EFL, Asyiah IN, Mudakir I, Harni R. 2022a. Role of mycorrhiza helper bacteria on mycorrhizal colonization and nematode Pratylenchus coffeae infection. Biotropia 29 (3): 244-253. DOI: 10.11598/btb.2022.29.3.1711.
Indonesian Ministry of Agriculture. 2019. Decree of the Minister of Agriculture Number 261 - KPTS - SR.310 - M - 4 - 2019 Concerning Minimum Technical Requirements for Organic Fertilizers, Biological Fertilizers, and Soil Conditioners. [Indonesian]
International Coffee Organization. 2022. Annual Review Coffee Year 2021/2022. https://www.ico.org/documents/cy2022-23/annual-review -2021-2022-e.pdf.
Jackson-Ziems T. 2016. Root-Lesion Nematodes. In: Harveson RM, Markell SG, Block CC, Gulya TJ (eds). Compendium of Sunflower Diseases and Pests. APS Online Publication. Saint Paul, Minnesota, US.
Jojima T, Inui M. 2015. Engineering the glycolytic pathway: A potential approach for improvement of biocatalyst performance. Bioengineered 6 (6): 328-334. DOI: 10.1080/21655979.2015.1111493.
Kalayu G. 2019. Phosphate solubilizing microorganisms: Promising approach as biofertilizers. Intl J Agron 2019 (1): 4917256. DOI: 10.1155/2019/4917256.
Khairul S-AM, Ainy MN, Faridah A, Jamaludin N-S, Ab Rashid N-KM. 2022. The proximate composition and metabolite profiling of sugarcane (Saccharum officinarum) molasses. Malays Appl Biol 51 (2): 63-68. DOI: 10.55230/mabjournal.v51i2.2259.
Kormanik P, Mc Graw A. 1982. Quantification of vesicular-arbuscular mycorrhizal in plant roots. In: Schenck NC (eds). Methods and Principles of Mycorrhizal Research, American Phytopathology Society, St. Paul.
Li H-B, Singh RK, Singh P, Song Q-Q, Xing Y-X, Yang L-T, Li Y-R. 2017. Genetic diversity of nitrogen-fixing and plant growth promoting Pseudomonas species isolated from sugarcane rhizosphere. Front Microbiol 8: 1268. DOI: 10.3389/fmicb.2017.01268.
Lyng M, Kovács ÁT. 2023. Frenemies of the soil: Bacillus and Pseudomonas interspecies interactions. Trends Microbiol 31 (8): 845-857. DOI: 10.1016/j.tim.2023.02.003.
Mozaheb N, Rasouli P, Kaur M, Van Der Smissen P, Larrouy-Maumus G, Mingeot-Leclercq M-P. 2023. A mildly acidic environment alters Pseudomonas aeruginosa virulence and causes remodeling of the bacterial surface. Microbiol Spectr 11 (4): e0483222. DOI: 10.1128/spectrum.04832-22.
Nasslahsen B, Prin Y, Ferhout H, Smouni A, Duponnois R. 2022. Mycorrhizae helper bacteria for managing the mycorrhizal soil infectivity. Front Soil Sci 2: 979246. DOI: 10.3389/fsoil.2022.979246.
Raimi A, Roopnarain A, Chirima GJ, Adeleke R. 2020. Insights into the microbial composition and potential efficiency of selected commercial biofertilisers. Heliyon 6 (7): e04342. DOI: 10.1016/j.heliyon.2020.e04342.
Sangwan S, Saxena G, Bana RS, Prasanna R. 2023. Regulatory role of arbuscular mycorrhiza fungi and helper bacteria associations in P and N dynamics in agriculture. Adv Microbiol Res 6: 026. DOI: 10.24966/AMR-694X/100026.
Scalzo R, Fibiano M, Pietromachi P, Mandala C, La Torre A. 2012. Effects of different fungicide treatments on grape, must and wine quality. Comm Agric Appl Biol Sci 77 (3): 151-161.
Schouteden N, De Waele D, Panis B, Vos CM. 2015. Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: A review of the mechanisms involved. Front Microbiol 6: 1280. DOI: 10.3389/fmicb.2015.01280.
Sui Q, Di F, Zhong H, Chen M, Wei Y. 2024. Molecular insight into the allocation of organic carbon to heterotrophic bacteria: Carbon metabolism and the involvement in nitrogen and phosphorus removal. Sci Total Environ 933: 173302. DOI: 10.1016/j.scitotenv.2024.173302.
Suryanti IAP, Santiasa IMPA. 2020. Macronutrients level and total of bacteria from combination of banana stems and coconut fibers with MA-11 as bioactivator. J Phys: Conf Ser 1503: 012039. DOI: 10.1088/1742-6596/1503/1/012039.
Tripathi R, Tewari R, Singh KP, Keswani C, Minkina T, Srivastava AK, De Corato U, Sansinenea E. 2022. Plant mineral nutrition and disease resistance: A significant linkage for sustainable crop protection. Front Plant Sci 13: 883970. DOI: 10.3389/fpls.2022.883970.
Turrini A, Avio L, Giovannetti M, Agnolucci M. 2018. Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: The challenge of translational research. Front Plant Sci 9: 1407. DOI: 10.3389/fpls.2018.01407.
Vaast P, Caswell-Chen EP, Zasoski RJ. 1998. Effects of two endoparasitic nematodes (Pratylenchus coffeae and Meloidogyne konaensis) on ammonium and nitrate uptake by Arabica coffee (Coffea arabica L.). Appl Soil Ecol 10: 171-178. DOI: 10.1016/S0929-1393(98)00037-7.
Van Bezooijen J. 2006. Methods and techniques for nematology. 2006. www.nematologia.com.br/files/tematicos/5.pdf
Verbruggen E, Röling WFM, Gamper HA, Kowalchuk GA, Verhoef HA, van der Heijden MGA. 2010. Positive effects of organic farming on below?ground mutualists: Large?scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol 186 (4): 968-979. DOI: 10.1111/j.1469-8137.2010.03230.x.
Xu J, Janahar JJ, Park HW, Balasubramaniam VM, Yousef AE. 2021. Influence of water activity and acidity on Bacillus cereus spore inactivation during combined high pressure-thermal treatment. LWT 146: 111465. DOI: 10.1016/j.lwt.2021.111465.
Yan F, Schubert S, Mengel K. 1996. Soil pH increases due to biological decarboxylation of organic anions. Soil Biol Biochem 28 (4-5): 617-624. DOI: 10.1016/0038-0717(95)00180-8.
Yan M, Wu M, Liu M, Li G, Liu K, Qiu C, Bao Y, Li Z. 2024. Comparative analysis on root exudate and rhizosphere soil bacterial assembly between tomatoes and peppers infected by Ralstonia. Chem Biol Technol Agric 11: 36. DOI: 10.1186/s40538-024-00561-5.