Evaluation of municipal sewage sludge for Arbuscular mycorrhizal fungi inoculum production

Abstract

This experiment was carried out to assess the effect of soil amendment with different concentrations of municipal sewage sludge (SS) as a substrate on inoculum production of two selected arbuscular mycorrhizal fungi (AMF) i.e., Glomus mosseae and Acaulospora laevis. The experiment was a 4 × 5 factorial design with four hosts including, maize (Zea mays L.), lemon grass (Cymbopogon nardus (L.) Rendle), palmarosa (Cymbopogon martini (Roxb.) Wats.) and Sesbania (Sesbania aculeata Poir.) and the following five SS concentrations 1) no substrate, 2) 25 g, 3) 50 g, 4) 75 g and 5) 200 g pot–1) with five replications. After 90 days, the host roots and its rhizosphere soil were examined for fungal mycorrhization in terms of percent of root colonization and AMF spore quantification. Furthermore, we calculated the response of each host in terms of increase in plant height (cm), root length (cm), root, fresh shoots, and dry weight (g). Mycorrhization pattern showed moderate to abundant intraradical mycelium, extraradical mycelium, vesicles, and arbuscules in all the host plants. This pattern varied with a change in the input level of SS. The 75 g treatment obtained the maximum mycorrhization of both the AMF, while the highest input level was detrimental to AMF and host plants' survival. Among the tested hosts, lemon grass and maize had a tremendous increment in G. mosseae and A. laevis inoculum respectively. Consequently, 75 g SS with lemon grass is the most compatible host–substrate combination capable of maximum G. mosseae and A. laevis spore production and root colonization and so far, highlights the significance of an alternative, cost–effective and affordable carrier medium that can be adopted by farmers as sustainable cultural practices for on farm AMF inoculum production.

Keywords

• Acaulospora laevis
• Agricultural waste
• Glomus mosseae
• Sludge utilization strategy
• Lemon grass

References

1. Al–Raddad, A.M., 1995. Mass production of Glomus mosseae spores. Mycorrhiza 5: 229–231.
2. Amir, H., Cavaloc, Y., Laurent, A., Pagand, P., Gunkel, P., Lemestre, M., Médevielle, V., Pain, A., McCoy, S., 2019. Arbuscular mycorrhizal fungi and sewage sludge enhance growth and adaptation of Metrosideros laurifolia on ultramafic soil in New Caledonia: A field experiment. Science of the Total Environment 651(1): 334–343.
3. Angle, J.S., Heckman, J.R., 1986. Effect of soil pH and sewage sludge on VA mycorrhizal infection of soybeans. Plant and Soil 93: 437–441.
4. Ansari, A.A., Jaikishun, S., 2011. Vermicomposting of sugarcane bagasse and rice straw and its impact on the cultivation of Phaseolus vulgaris L. in Guyana, South America. Journal of Agricultural Technology 7(2): 225–234.
5. Aslantas, R., Angin, I., Karakurt, H., Kose, M., 2010. Vegetative and pomological changes of sour cherry as affected by sewage sludge application. Bulgarian Journal of Agricultural Science 16(6): 740–747.
6. Bettiol, W., Ghini, R., 2011. Impacts of sewage sludge in tropical soil: A case study in Brazil. Applied and Environmental Soil Science Article ID 212807.
7. Bhowmik, S.N., Yadav, G.S., Datta, M., 2015. Rapid mass multiplication of Glomus mosseae inoculum as influenced by some biotic and abiotic factors. Bangladesh Journal of Botany 44: 209–214.
8. Burducea, M., Lobiuc, A., Asandulesa, M., Zaltariov, M.F., Burducea, I., Popescu, S.M., Zheljazkov, V.D., 2019. Effects of sewage sludge amendments on the growth and physiology of sweet basil. Agronomy 9(9): 548.

9. Carrenho, R., Trufem, S.F.B., Bononi, V.L.R., 2001. Arbuscular mycorrhizal fungi in rhizospheres of three phytobionts established in a revegetated riparian area. Acta Botanica Brasilica 15(1): 115–124.
10. del Val, C., Barea, J.M., Azcón–Aguilar, C., 1999. Assessing the tolerance to heavy metals of arbuscular mycorrhizal fungi isolated from sewage sludge-contaminated soils. Applied Soil Ecology 11(2–3): 261–269.
11. Dolgen, D., Alpaslan, M.N., Delen, N., 2004. Use of an agro-industry treatment plant sludge on iceberg lettuce growth. Ecological Engineering 23: 117–125.
12. Douds, D.D., Schenck, N.C., 1990. Relationship of colonization and sporulation by VA mycorrhizal fungi to plant nutrient and carbohydrate contents. New Phytology 116: 621–627.
13. Eid, E.M., Hussain, A.A., Taher, M.A., Galal, T.M., Shaltout, K.H., Sewelam, N., 2020. Sewage sludge application enhances the growth of Corchorus olitorius Plants and provides a sustainable practice for nutrient recirculation in agricultural soils. Journal of Soil Science and Plant Nutrition 20: 149–159.
14. Feldmann, F., Grotkass, C., 2002. Directed inoculum production–shall we be able to design populations of arbuscular mycorrhizal fungi to achieve predictable symbiotic effectiveness? In: Mycorrhizal Technology in Agriculture. Gianinazzi, S., Schüepp, H., Barea, J.M., Haselwandter, K. (Eds.). Birkhäuser, Basel. pp. 261–279.
15. Feldmann, F., Hallmann, J., Wagner, S., Long, X.Q., Yang, R., Schneider, C., Hutter, I., Ceipek, B., Fan, J., Zheng, X., Wang, C., Feng, G., 2008. Mycorrhizal fungi as biological components of the integrated cucumber production (BIOMYC)–promising results for mycorrhizal technology transfer to horticultural practice. In: Mycorrhiza Works. Feldmann, F., Kapulnik, Y., Baar, J. (Eds.). Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany. pp. 25–38.
16. Gaur, A., Adholeya, A., 2000. Effects of particle size of soil–less substrates upon AM fungal inoculum production. Mycorrhiza 10: 43–48.
17. Gerdemann, J.W., Nicolson, Y.H., 1963. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society 46: 235–244.
18. Gianinnazi, S., Vosatka, M., 2004. Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Canadian Journal of Botany 982: 1264–1271.
19. Gill, T.S., Singh, R.S., 2001. Effect of host and substrates on development of VA mycorrhizal colonization and sporulation of Glomus fasciculatum. Indian Phytopathology 5(2): 261–263.
20. Gómez–Bellot, M.J., Lorente, B., Sánchez–Blanco, M.J., Ortuño, M.F., Nortes, P.A., Alarcón, J.J., 2020. Influence of mixed substrate and arbuscular mycorrhizal fungi on photosynthetic efficiency, nutrient and water status and yield in tomato plants irrigated with saline reclaimed waters. Water 12(2): 438.
21. Gupta, M.M., 2017. Differential response of arbuscular mycorrhizal sporocarps in long–term trap culturing. Phytomorphology 67(1&2): 27-34.
22. Haghighi, M., 2011. Sewage sludge application in soil improved leafy vegetable growth. Journal of Biological and Environmental Sciences 5(15): 165–167.
23. Hoagland, D.R., Arnon, D.I., 1950. The water–culture method for growing plants without soil. University of California, College of Agriculture, Agricultural Experiment Station, Berkeley, California, USA. Circular No. 347, 32p. Available at [Access date : 01.04.2021]: http://hdl.handle.net/2027/uc2.ark:/13960/t51g1sb8j
24. Kapoor, R., Sharma, D., Bhatnagar, A.K., 2008. Arbuscular mycorrhizae in micropropagation systems and their potential applications. Scientia Horticulturae 116: 227–239.
25. Kaushish, S., Kumar, A., Mangla, C., Aggarwal, A., 2011. Mass multiplication of AM inoculum: effect of hosts and substrates in rapid culturing of Acaulospora laevis. Indian Phytopathology 64(2): 159–163.
26. Kicińska, A., Gucwa, J., Kosa–Burda, B., 2019. Evaluating Potential for using municipal sewage sludge in the rehabilitation of ground degraded by the sodium processing industry. Bulletin of Environmental Contamination and Toxicology 102: 399–406.
27. Koide, R.T., Schreiner, R.P., 1992. Regulation of the vesicular–arbuscular mycorrhizal symbiosis. Annual Review of Plant Physiology and Plant Molecular Biology 43: 557–581.
28. Kokkoris, V., Hart, M., 2019.. In vitro propagation of arbuscular mycorrhizal fungi may drive fungal evolution. Frontiers in Microbiology 10: 2420.
29. Liu, R., Wang, F., 2003. Selection of appropriate host plants used in trap culture of arbuscular mycorrhizal fungi. Mycorrhiza 13: 123–127.
30. Lobo, T.F., Filho, H.G., 2009. Sewage sludge levels on the development and nutrition of sunflower plants. Soil Science and Plant Nutrition 9(3): 245–255.
31. Maiti, D., 2011. Improving activity of native arbuscular mycorrhizal fungi (AMF) for mycorrhizal benefits in agriculture: Status and prospect. Journal of Biofertilizers and Biopesticides S1: 001.
32. Menge, J.A., Timmer, L.W., 1982. Procedure for inoculation of plants with VAM in the laboratory, greenhouse and field. In: Methods and Principles of Mycorrhizal Research, Schenck, N.C. (Ed.). American Phytopathology Society, St. Paul, MN. pp. 59–68.
33. Mhlongo, M.I., Piater, L.A., Madala, N.E., Labuschagne, N., Dubery, I.A., 2018. The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Frontiers in Plant Science 9: 112.
34. Moreira, B.C., Junior, P.P., Jordão, T.C., Silva, M.C.S., Ribeiro, A.P.F., Stürmer, S.L., Salomão, L.C.C., Otoni, W.C., Kasuya, M.C.M., 2019. Effect of inoculation of pineapple plantlets with arbuscular mycorrhizal fungi obtained from different inoculum sources multiplied by the on–farm method. Revista Brasileira de Ciência do Solo 43:e0180148.
35. Mukerji, K.G., Manoharachary, C., Chamola, B.P., 2002. Techniques in Mycorrhizal Studies, 2nd Edition, Kluwer Academic Publishers, The Netherlands. 553p.
36. Mukhongo, R.W., Tumuhairwe, J.B., Ebanyat, P., AbdelGadir, A.H., Thuita, M., Masso, C., 2016. Production and use of arbuscular mycorrhizal fungi inoculum in Sub–Saharan Africa: challenges and ways of improving. International Journal of Soil Science 11: 108–122.
37. Nzanza, B., Marais, D., Soundy, P., 2011. Response of tomato (Solanum lycopersicum L.) to nursery inoculation with Trichoderma harzianum and arbuscular mycorrhizal fungi under field conditions. Acta Agriculturae Scandinavica B–Soil and Plant Science 63(3): 209–215.
38. Oladejo, J., Shi, K., Luo, X., Yang, G., Wu, T., 2019. A Review of Sludge–to–Energy Recovery Methods. Energies 12(1): 60.
39. Oleszczuk, P., Malara, A., Jośko, I., Lesiuk, A., 2012. The phytotoxicity changes of sewage sludge–amended soils. Water, Air, and Soil Pollution 223: 4937–4948.
40. Phillips, J.M., Hayman, D.S., 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55: 158–161.
41. Pöykiö, R., Watkins, G., Dahl, O., 2019. Characterisation of municipal sewage sludge as a soil ımprover and a fertilizer product. Ecological Chemistry and Engineering S 26(3): 547–557.
42. Rodrigues, K.M., Rodrigues, B.F., 2017. Development of carrier based in vitro produced arbuscular mycorrhizal (AM) fungal inocula for organic agriculture. Annals of Advanced Agricultural Sciences 1(1): 26–37.
43. Rosiek, K., 2020. Directions and challenges in the management of municipal sewage sludge in Poland in the context of the circular economy. Sustainability 12(9): 3686.
44. Ryan, M.H., Graham, J.H., 2002. Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant and Soil 244: 263–271.
45. Schenck, N.C., Perez, Y., 1990. Manual for the identification of VA mycorrhizal (VAM) fungi. 3rd Edition, Synergistic Publications, Florida, USA. 286p.
46. Schlemper, R.T., Stürmer, S.L., 2014. On farm production of arbuscular mycorrhizal fungi inoculum using lignocellulosic agrowastes. Mycorrhiza 24(8): 571–580.
47. Selvakumar, G., Kim, K., Walitang, D., Chanratana, M., Kang, Y., Chung, B., Sa, T., 2016. Trap culture technique for propagation of arbuscular mycorrhizal fungi using different host plants. Korean Journal of Soil Science and Fertilizer 49(5): 608–613.
48. Selvakumar, G., Shagol, C.C., Kim, K., Han, S., Sa, T., 2018. Spore associated bacteria regulates maize root K+/Na+ ion homeostasis to promote salinity tolerance during arbuscular mycorrhizal symbiosis. BMC Plant Biology 18(1): 109.
49. Simpson, D., Daft, M.J., 1990. Interactions between water–stress and different mycorrhizal inocula on plant growth and mycorrhizal development in maize and sorghum. Plant and Soil 121: 179–186.
50. Singh, R.P., Agrawal, M., 2010. Effect of different sewage sludge applications on growth and yield of Vigna radiata L. field crop: Metal uptake by plant. Ecological Engineering 36(7): 969–972.
51. Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis, 3rd Edition, Academic Press, London, UK. 803p.
52. Sreenivasa, M.N., Bagyaraj, D.J., 1988. Selection of a suitable substrate for mass multiplication of Glomus fasciculatum. Plant and Soil 109: 125–127.
53. Sullivan, T.S., Stromberger, M.E., Paschke, M.W., 2006. Parallel shifts in plant and soil microbial communities in response to biosolids in a semi–arid grassland. Soil Biology and Biochemistry 38: 449–459.
54. Tahat, M.M., Sijam, K., 2012. Mycorrhizal fungi and abiotic environmental conditions relationship. Research Journal of Environmental Sciences 6(4): 125–133.
55. Tanwar, A., Aggarwal, A., Yadav, A., Parkash, V., 2013. Screening and selection of efficient host and sugarcane bagasse as substrate for mass multiplication of Funneliformis mosseae. Biological Agriculture and Horticulture 29(2): 107–117.
56. Tariq, U., Rehman, S., Khan, M.A., Younis, A., 2012. Agricultural and municipal waste as potting media components for the growth and fl owering of Dahlia hortensis ‘Figaro’. Turkish Journal of Botany 36: 378–385.
57. Uko, A.E., Effa, E.B., Isong, I.A., Effiong, J.E., 2020. Yield performance and leaf nutrient composition of bambara groundnut under arbuscular mycorrhizal inoculation in a poultry manure amended ultisol. Pakistan Journal of Biological Sciences 23: 1397–1407.
58. Wei, Y., Liu, Y., 2005. Effects of sewage sludge compost application on crops and cropland in a 3–year field study. Chemosphere 59(9): 1257–1265.
59. Whiteside, M.D., Werner, G.D.A., Caldas, V.E.A., van’t Padje, A., Dupin, S.E., Elbers, B., Bakker, M., Wyatt, G.A.K., Klein, M., Hink, M.A., Postma, M., Vaitla, B., Noë, R., Shimizu, T.S., West, S.A., Kiers, E.T., 2019. Mycorrhizal fungi respond to resource ınequality by moving phosphorus from rich to poor patches across networks. Current Biology 29(12): 2043–2050.