Abstract
Soil is home to microbiota with diverse metabolic activities. These microorganisms play vital roles in many ecological processes. Thus, the assessment of microbial functional diversity is an important quality indicator of soil ecosystems. In this study, we collected soil samples from three distinct forest habitats, i.e., an agroforest, a primary forest (PF), and a secondary forest, within the Angat Watershed Reservation in Bulacan, Northern Philippines. Community-level physiological profiling (CLPP) was done with the BIOLOG EcoPlate™ to analyze the responses of the soil microbial communities from the three forest habitats in the absence or presence of antibiotics. The BIOLOG EcoPlate represents 31 utilizable carbon sources. Based on the CLPP analysis, soil samples from the PF showed significantly higher utilization of most carbon sources than the other forest types (p < 0.05). Thus, less disturbed forest types constitute more functionally diverse microbial communities. The presence of antibiotics significantly decreased the carbon utilization patterns of the soil microbial communities (p < 0.05), indicating the possible use of CLPP in monitoring contamination in soil.
References
Doran JW, Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Appl Soil Ecol 15:3–11. https://doi.org/10.1016/S0929-1393(00)00067-6
Grzadziel J, Furtak K, Galazka A (2018) Community-level physiological profiles of microorganisms from different types of soil that are characteristic to poland-a long-term microplot experiment. Sustainability. https://doi.org/10.3390/su11010056
Raynaud X, Nunan N (2014) Spatial ecology of bacteria at the microscale in soil. PLoS ONE. https://doi.org/10.1371/journal.pone.0087217
Gałązka A, Furtak K (2019) Functional microbial diversity in context to agriculture. In: Das S, Dash HR (eds) Microbial diversity in the genomic era. Academic Press, New York, pp 347–358
Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomos JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Method 58:169–188. https://doi.org/10.1016/j.mimet.2004.04.006
Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions. Appl Environ Microbiol 68:2391–2396. https://doi.org/10.1128/AEM.68.5.2391-2396.2002
Chaudhary DK, Khulan A, Kim J (2019) Development of a novel cultivation technique for uncultured soil bacteria. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-019-43182-x
Banaay CGB, Cruz CMV, Cuevas VC (2013) Effect of organic matter amendment on the rhizosphere microbial community and root-infecting pathogens of aerobic rice variety Apo. Philipp Sci Lett 6:107–118
Chodak M, Pietrzykowski M, Sroka K (2015) Physiological profiles of microbial communities in mine soils afforested with different tree species. Ecol Eng 81:462–470. https://doi.org/10.1016/j.ecoleng.2015.04.077
Siles JA, Cajthaml T, Filipová A, Minerbi S, Margesin R (2017) Altitudinal, seasonal and interannual shifts in microbial communities and chemical composition of soil organic matter in Alpine forest soils. Soil Biol Biochem 112:1–13. https://doi.org/10.1016/j.soilbio.2017.04.014
Maillard F, Leduc V, Bach C, Reichard A, Fauchery L, Saint-André L, Zeller B, Buée M (2019) Soil microbial functions are affected by organic matter removal in temperate deciduous forest. Soil Biol Biochem 133:28–36. https://doi.org/10.1016/j.soilbio.2019.02.015
Feigl V, Ujaczki É, Vaszita E, Molnár M (2017) Influence of red mud on soil microbial communities: application and comprehensive evaluation of the BIOLOG EcoPlate approach as a tool in soil microbiological studies. Sci Total Environ 595:903–911. https://doi.org/10.1016/j.scitotenv.2017.03.266
Siles JA, Öhlinger B, Cajthaml T, Kistler E, Margesin R (2018) Characterization of soil bacterial, archaeal, and fungal communities inhabiting archaeological human-impacted layers at Monte Iato settlement (Sicily, Italy). Sci Rep 8:1–14. https://doi.org/10.1038/s41598-018-20347-8
Barreiro A, Fontúrbel MT, Lombao A, Martín A, Vega JA, Fernández C, Carballas T, Díaz-Raviña M (2015) Using phospholipid fatty acid and community level physiological profiling techniques to characterize soil microbial communities following an experimental fire and different stabilization treatments. CATENA 135:419–429. https://doi.org/10.1016/j.catena.2014.07.011
Xu W, Ge Z, Poudel DR (2015) Application and optimization of BIOLOG EcoPlates in functional diversity studies of soil microbial communities. MATEC Web Conf 22:1–6. https://doi.org/10.1051/matecconf/20152204015
Pinna VM, Castaldi P, Deiana P, Pusino A, Garau G (2012) Sorption behavior of sulfamethazine on unamended and manure-amended soils and short-term impact on soil microbial community. Ecotoxicol Environ Saf 84:234–242. https://doi.org/10.1016/j.ecoenv.2012.07.006
Liu B, Li Y, Zhang X, Wang J, Gao M (2015) Effects of chlortetracycline on soil microbial communities: comparisons of enzyme activities to the functional diversity via BIOLOG EcoPlates™. Eur J Soil Biol 68:69–76. https://doi.org/10.1016/j.ejsobi.2015.01.002
Ma T, Pan X, Chen L, Liu W, Christie P, Luo Y, Wu L (2016) Effects of different concentrations and application frequencies of oxytetracycline on soil enzyme activities and microbial community diversity. Eur J Soil Biol 76:53–60. https://doi.org/10.1016/j.ejsobi.2016.07.004
Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilization profiles—a critique. FEMS Microbiol Ecol 42:1–14
Mann A, Nehra K, Rana JS, Dahiya T (2021) Antibiotic resistance in agriculture: perspectives on upcoming strategies to overcome upsurge in resistance. Curr Res Microb Sci 2:100030. https://doi.org/10.1016/j.crmicr.2021.100030
da Silva FL, de Lima BR, da Silva BA, Volcão LM, da Silva Júnior FMR, Ramos DF (2023) Assessment of the impact of ceftriaxone on the functional profile of soil microbiota using BIOLOG EcoPlate™. Soil Syst 7:55. https://doi.org/10.3390/soilsystems7020055
Garland JL (1997) Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol 24:289–300
Xu Y, Yu W, Ma Q, Wang J, Zhou H, Jiang C (2016) The combined effect of sulfadiazine and copper on soil microbial activity and community structure. Ecotoxicol Environ Saf 134:43–52. https://doi.org/10.1016/j.ecoenv.2016.06.041
Sang X, Li K, Zhu Y, Ma X, Hao H, Bi J, Zhang G, Hou H (2020) The impact of microbial diversity on biogenic amines formation in grasshopper sub shrimp paste during fermentation. Front Microbiol 11:782. https://doi.org/10.3389/fmicb.2020.00782
Beaumont M, Roura E, Lambert W, Turni C, Michiels J, Chalvon-Demersay T (2022) Selective nourishing of gut microbiota with amino acids: a novel prebiotic approach? Front Nutr. https://doi.org/10.3389/fnut.2022.1066898
Shrestha K, Stevens S, Shrestha P, Adetutu EM, Walsh KB, Ball AS, Midmore DJ (2015) Characterization of the soil microbial community of cultivated and uncultivated vertisol in Australia under several management regimes. Agric Ecosyst Environ 199:418–427. https://doi.org/10.1016/j.agee.2014.10.002
Ravindra PS, Bhardwaj A (2023) β-glucans: a potential source for maintaining gut microbiota and the immune system. Front Nutr 10:1143682. https://doi.org/10.3389/fnut.2023.1143682
Groisillier A, Labourel A, Michel G, Tonon T (2015) The mannitol utilization system of the marine bacterium Zobellia galactanivorans. Appl Environ Microbiol 81:1799–1812. https://doi.org/10.1128/aem.02808-14
Sun J, Li S, Fan C, Cui K, Tan H, Liao Q, Lu L (2022) N-Acetylglucosamine promotes tomato plant growth by sha** the community structure and metabolism of the rhizosphere microbiome. Microbiol Spectr. https://doi.org/10.1128/spectrum.00358-22
Ucar RA, Pérez-Díaz IM, Dean LL (2020) Gentiobiose and cellobiose content in fresh and fermenting cucumbers and utilization of such disaccharides by lactic acid bacteria in fermented cucumber juice medium. Food Sci Nutr 8:5798–5810. https://doi.org/10.1002/fsn3.1830
Klimek B, Chodak M, Jaźwa M, Solak A, Tarasek A, Niklińska M (2016) The relationship between soil bacteria substrate utilisation patterns and the vegetation structure in temperate forests. Eur J For Res 135:179–189. https://doi.org/10.1007/s10342-015-0929-4
Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles, and fate of organic acids in soils: a review. S Afr J Bot 108:393–406. https://doi.org/10.1016/j.sajb.2016.09.002
Zhu T, Zhang B, Feng Y, Li Z, Tang X, Ban X, Kong H, Li C (2022) Beneficial effects of three dietary cyclodextrins on preventing fat accumulation and remodeling gut microbiota in mice fed a high-fat diet. Foods 11:1118. https://doi.org/10.3390/foods11081118
Reitermayer D, Kafka TA, Lenz CA, Vogel RF (2018) Interrelation between Tween and the membrane properties and high-pressure tolerance of Lactobacillus plantarum. BMC Microbiol 18:72. https://doi.org/10.1186/s12866-018-1203-y
Banning NC, Lalor BM, Cookson WR, Grigg AH, Murphy DV (2012) Analysis of soil microbial community level physiological profiles in native and post-mining rehabilitation forest: which substrates discriminate? Appl Soil Ecol 56:27–34. https://doi.org/10.1016/j.apsoil.2012.01.009
Klimek B, Chodak M, Jaźwa M, Niklińska M (2016) Functional diversity of soil microbial communities in boreal and temperate scots pine forests. Eur J For Res 135:731–742. https://doi.org/10.1007/s10342-016-0968-5
Sofo A, Ricciuti P (2019) A standardized method for estimating the functional diversity of soil bacterial community by BIOLOG EcoPlates™ assay—The case study of a sustainable olive orchard. Appl Sci 9:4035. https://doi.org/10.3390/app9194035
Gajda AM, Czyż EA, Furtak K, Jończyk K (2019) Effects of crop production practices on soil characteristics and metabolic diversity of microbial communities under winter wheat. Soil Res 57:124–131. https://doi.org/10.1071/SR18113
Chinthalapudi DPM, Pokhrel S, Kingery WL, Shankle MW, Ganapathi Shanmugam S (2023) Exploring the synergistic impacts of cover crops and fertilization on soil microbial metabolic diversity in dryland soybean production systems using BIOLOG EcoPlates. Appl Biosci 2:328–346. https://doi.org/10.3390/applbiosci2030022
Zhang B-H, Hong J-P, Zhang Q, ** D-S, Gao C-H (2020) Contrast in soil microbial metabolic functional diversity to fertilization and crop rotation under rhizosphere and non-rhizosphere in the coal gangue landfill reclamation area of Loess Hills. PLoS ONE 15:e0229341. https://doi.org/10.1371/journal.pone.0229341
Muñiz S, Lacarta J, Pata MP, Jimenez JJ, Navarro E (2014) Analysis of the diversity of substrate utilisation of soil bacteria exposed to Cd and earthworm activity using generalised additive models. PLoS ONE 9:e85057. https://doi.org/10.1371/journal.pone.0085057
Borgulat J, Łukasik W, Borgulat A, Nadgórska-Socha A, Kandziora-Ciupa M (2021) Influence of lead on the activity of soil microorganisms in two Beskidy landscape parks. Environ Monit Assess 193:839. https://doi.org/10.1007/s10661-021-09503-2
Acknowledgements
The authors would like to thank the National Power Corporation—Angat Watershed Area for providing the necessary permit and assistance during the soil sample collection.
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Decena, B.C., dela Cruz, T.E.E. Detection of Changes in Soil Microbial Community Physiological Profiles in Relation to Forest Types and Presence of Antibiotics Using BIOLOG EcoPlate. Indian J Microbiol 64, 773–779 (2024). https://doi.org/10.1007/s12088-024-01294-7
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DOI: https://doi.org/10.1007/s12088-024-01294-7