Abstract
The continuous increment in world population coupled with the greatest natural resource consumption and waste generation has an enormous impact on the environment. To date, using biological indicators (bioindicators) to evaluate the biological quality of natural environments is very common. Nonetheless, selecting those suitable for each ecosystem or contaminant is one of the most important issues for environmental sciences. Bacteria and helminths are mainly related to fecal contamination, while antibiotic-resistant bacteria, fungi, viruses, and microalgae are organisms used to determine deteriorated ecosystems by diverse contaminants. Nowadays, each bioindicator is used as a specific agent of different contaminant types, but detecting and quantifying these bioindicator microorganisms can be performed from simple microscopy and culture methods up to a complex procedure based on omic sciences. Developing new techniques based on the metabolism and physiological responses of traditional bioindicators is shown in a fast environmental sensitivity analysis. Therefore, the present review focuses on analyzing different bioindicators to facilitate developing suitable monitoring environmental systems according to different pollutant agents. The traditional and new methods proposed to detect and quantify different bioindicators are also discussed. Their vital role is considered in implementing efficient ecosystem bioprospection, restoration, and conservation strategies directed to natural resource management.
Similar content being viewed by others
Data availability
The datasets used or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Abrego, N., Crosier, B., Somervuo, P., Ivanova, N., Abrahamyan, A., Abdi, A., Hämäläinen, K., Junninen, K., Maunula, M., Purhonen, J., & Ovaskainen, O. (2020). Fungal communities decline with urbanization—more in air than in soil. The ISME Journal, 14(11), 2806–2815. https://doi.org/10.1038/s41396-020-0732-1
Ahmed, W., Toze, S., Veal, C., Fisher, P., Zhang, Q., Zhu, Z., Staley, C., & Sadowsky, M. J. (2021). Comparative decay of culturable faecal indicator bacteria, microbial source tracking marker genes, and enteric pathogens in laboratory microcosms that mimic a sub-tropical environment. Science of the Total Environment, 751, 141475. https://doi.org/10.1016/j.scitotenv.2020.141475
Ajonina, C., Buzie, C., Rubiandini, R. H., & Otterpohl, R. (2015). Microbial pathogens in wastewater treatment plants (WWTP) in Hamburg. Journal of Toxicology and Environmental Health, Part A, 78(6), 381–387. https://doi.org/10.1080/15287394.2014.989626
Amoah, I. D., Kumari, S., Reddy, P., Stenström, T. A., & Bux, F. (2020). Impact of informal settlements and wastewater treatment plants on helminth egg contamination of urban rivers and risks associated with exposure. Environmental Monitoring and Assessment, 192, 1–13. https://doi.org/10.1007/s10661-020-08660-0
Anders, J. L., Nakao, M., Uchida, K., Ayer, C. G., Asakawa, M., & Koizumi, I. (2019). Comparison of the intestinal helminth community of the large Japanese field mouse (Apodemus speciosus) between urban, rural, and natural sites in Hokkaido, Japan. Parasitology International, 70, 51–57. https://doi.org/10.1016/j.parint.2019.02.001
Angelescu, D. E., Huynh, V., Hausot, A., Yalkin, G., Plet, V., Mouchel, J. M., Guérin-Rechdaoui, R., Azimi, S., & Rocher, V. (2019). Autonomous system for rapid field quantification of Escherichia coli in surface waters. Journal of Applied Microbiology, 126(1), 332–343. https://doi.org/10.1111/jam.14066
Bagi, A., Knapik, K., & Baussant, T. (2022). Abundance and diversity of n-alkane and PAH-degrading bacteria and their functional genes–Potential for use in detection of marine oil pollution. Science of the Total Environment, 810, 152238. https://doi.org/10.1016/j.scitotenv.2021.152238
Bai, Y., Wang, Q., Liao, K., Jian, Z., Zhao, C., & Qu, J. (2018). Fungal community as a bioindicator to reflect anthropogenic activities in a river ecosystem. Frontiers in Microbiology, 9, 3152. https://doi.org/10.3389/fmicb.2018.03152
Bain, R., Cronk, R., Wright, J., Yang, H., Slaymaker, T., & Bartram, J. (2014). Fecal contamination of drinking-water in low-and middle-income countries: A systematic review and meta-analysis. PLoS Medicine, 11(5), e1001644. https://doi.org/10.1371/journal.pmed.1001644
Behere, M. J., Shinde, A. H., & Haldar, S. (2023). Determination of antibiotic resistance profile of bacterial community from environmental water using antibiotic-resistant bacterial contamination detection (ABCD) kit. Biosensors and Bioelectronics, 221, 114943. https://doi.org/10.1016/j.bios.2022.114943
Besant, J. D., Sargent, E. H., & Kelley, S. O. (2015). Rapid electrochemical phenotypic profiling of antibiotic-resistant bacteria. Lab on a Chip, 15(13), 2799–2807. https://doi.org/10.1039/c5lc00375j
Bigham, T., Casimero, C., Dooley, J. S., Ternan, N. G., Snelling, W. J., & Davis, J. (2019). Microbial water quality: Voltammetric detection of coliforms based on riboflavin–ferrocyanide redox couples. Electrochemistry Communications, 101, 99–103. https://doi.org/10.1016/j.elecom.2019.02.022
Bilous, O. P., Barinova, S. S., Ivanova, N. O., & Huliaieva, O. A. (2016). The use of phytoplankton as an indicator of internal hydrodynamics of a large seaside reservoir–case of the Sasyk Reservoir, Ukraine. Ecohydrology & Hydrobiology, 16(3), 160–174. https://doi.org/10.1016/j.ecohyd.2016.08.002
Bonanno, G., Veneziano, V., & Piccione, V. (2020). The alga Ulva lactuca (Ulvaceae, Chlorophyta) as a bioindicator of trace element contamination along the coast of Sicily, Italy. Science of The Total Environment, 699, 134329. https://doi.org/10.1016/j.scitotenv.2019.134329
Bucci, A., Petrella, E., Naclerio, G., Allocca, V., & Celico, F. (2015). Microorganisms as contaminants and natural tracers: A 10-year research in some carbonate aquifers (southern Italy). Environmental Earth Sciences, 74, 173–184. https://doi.org/10.1007/s12665-015-4043-1
Calderon, J. S., Verbyla, M. E., Gil, M., Pinongcos, F., Kinoshita, A. M., & Mladenov, N. (2022). Persistence of fecal indicators and microbial source tracking markers in water flushed from riverbank soils. Water, Air, & Soil Pollution, 233(3), 83. https://doi.org/10.1007/s11270-022-05542-8
Canh, V. D., Torii, S., Furumai, H., & Katayama, H. (2021). Application of capsid integrity (RT-) qPCR to assessing occurrence of intact viruses in surface water and tap water in Japan. Water Research, 189, 116674. https://doi.org/10.1016/j.watres.2020.116674
Ceulemans, T., Van Geel, M., Jacquemyn, H., Boeraeve, M., Plue, J., Saar, L., Kasari, L., Peeters, G., Acker, K. V., Crauwels, S., Lievens, B., & Honnay, O. (2019). Arbuscular mycorrhizal fungi in European grasslands under nutrient pollution. Global Ecology and Biogeography, 28(12), 1796–1805. https://doi.org/10.1111/geb.12994
Chen, L., Hu, B. X., Dai, H., Zhang, X., Xia, C. A., & Zhang, J. (2019). Characterizing microbial diversity and community composition of groundwater in a salt-freshwater transition zone. Science of the Total Environment, 678, 574–584. https://doi.org/10.1016/j.scitotenv.2019.05.017
Cudowski, A., Pietryczuk, A., & Hauschild, T. (2015). Aquatic fungi in relation to the physical and chemical parameters of water quality in the Augustów Canal. Fungal Ecology, 13, 193–204. https://doi.org/10.1016/j.funeco.2014.10.002
Cui, H., Yang, K., Pagaling, E., & Yan, T. (2013). Spatial and temporal variation in enterococcal abundance and its relationship to the microbial community in Hawaii beach sand and water. Applied and Environmental Microbiology, 79(12), 3601–3609. https://doi.org/10.1128/AEM.00135-13
Das, S., Lizon, F., Gevaert, F., Bialais, C., Duong, G., Ouddane, B., & Souissi, S. (2023). Assessing indicators of arsenic toxicity using variable fluorescence in a commercially valuable microalgae: Physiological and toxicological aspects. Journal of Hazardous Materials, 452, 131215. https://doi.org/10.1016/j.jhazmat.2023.131215
Dell’Aglio, E., Cosentino, F., & Campanella, L. (2017). Use of algae Scenedesmus as bioindicators of water pollution from active ingredients. Journal of Analytical & Pharmaceutical Research, 6(5), 00189. https://doi.org/10.15406/japlr.2017.06.00189
Duarte, G. S. C., Lehun, A. L., Leite, L. A. R., Consolin-Filho, N., Bellay, S., & Takemoto, R. M. (2020). Acanthocephalans parasites of two Characiformes fishes as bioindicators of cadmium contamination in two neotropical rivers in Brazil. Science of the Total Environment, 738, 140339. https://doi.org/10.1016/j.scitotenv.2020.140339
Erdem, Ö., Saylan, Y., Cihangir, N., & Denizli, A. (2019). Molecularly imprinted nanoparticles based plasmonic sensors for real-time Enterococcus faecalis detection. Biosensors and Bioelectronics, 126, 608–614. https://doi.org/10.1016/j.bios.2018.11.030
Ferrer-Vilanova, A., Alonso, Y., Ezenarro, J., & J., Santiago, S., Muñoz-Berbel, X., & Guirado, G. (2021). Electrochromogenic detection of live bacteria using soluble and insoluble Prussian blue. ACS Omega, 6(46), 30989–30997. https://doi.org/10.1021/acsomega.1c03434
Fongaro, G., García-González, M. C., Hernández, M., Kunz, A., Barardi, C. R., & Rodríguez-Lázaro, D. (2017). Different behavior of enteric bacteria and viruses in clay and sandy soils after biofertilization with swine digestate. Frontiers in Microbiology, 8, 74. https://doi.org/10.3389/fmicb.2017.00074
Frick, C., Vierheilig, J., Linke, R., Savio, D., Zornig, H., Antensteiner, R., Baumgarther, C., Bucher, C., Blaschke, A. P., Derx, J., Kirschner, A. K. T., Ryzinska-Paier, G., Mayer, R., Seidl, D., Nadiotis-Tsaka, T., Sommer, R., & Farnleitner, A. H. (2018). Poikilothermic animals as a previously unrecognized source of fecal indicator bacteria in a backwater ecosystem of a large river. Applied and Environmental Microbiology, 84(16), e00715–e00718. https://doi.org/10.1128/AEM.00715-18
Fu, J., Chiang, E. L. C., Medriano, C. A. D., Li, L., & Bae, S. (2021). Rapid quantification of fecal indicator bacteria in water using the most probable number-loop-mediated isothermal amplification (MPN-LAMP) approach on a polymethyl methacrylate (PMMA) microchip. Water Research, 199, 117172. https://doi.org/10.1016/j.watres.2021.117172
Garcia, A. N., Stein, E. M., Villela, L. Z., Yokoya, N. S., Neto, P. C., & de Carvalho, L. R. (2020). Dichotomaria marginata (Rhodophyta) as a bioindicator for marine pollution: An overview about its metabolites and adsorbed pollutants. Revista de Biología Marina y Oceanografía, 55(2), 128–141. https://doi.org/10.22370/rbmo.2020.55.2.2498
Giorgio, A., De Bonis, S., & Guida, M. (2016). Macroinvertebrate and diatom communities as indicators for the biological assessment of river Picentino (Campania, Italy). Ecological Indicators, 64, 85–91. https://doi.org/10.1016/j.ecolind.2015.12.001
Guo, F., Gai, W. P., Hong, Y., Tang, B. Z., Qin, J., & Tang, Y. (2015). Aggregation-induced emission fluorogens as biomarkers to assess the viability of microalgae in aquatic ecosystems. Chemical Communications, 51(97), 17257–17260. https://doi.org/10.1039/c5cc07012k
Gyawali, P., Croucher, D., Ahmed, W., Devane, M., & Hewitt, J. (2019). Evaluation of pepper mild mottle virus as an indicator of human faecal pollution in shellfish and growing waters. Water Research, 154, 370–376. https://doi.org/10.1016/j.watres.2019.02.003
Han, S., Zhang, Q., Zhang, X., Liu, X., Lu, L., Wei, J., Li, Y., Wang, Y., & Zheng, G. (2019). A digital microfluidic diluter-based microalgal motion biosensor for marine pollution monitoring. Biosensors and Bioelectronics, 143, 111597. https://doi.org/10.1016/j.bios.2019.111597
Hariyati, R., & Putro, S. P. (2019). Bioindicator for environmental water quality based on saprobic and diversity indices of planktonic microalgae: A study case at Rawapening lake, Semarang district, Central Java, Indonesia. Journal of Physics: Conference Series, 1217(1), 012130. https://doi.org/10.1088/1742-6596/1217/1/012130
Hruby, C. E., Soupir, M. L., Moorman, T. B., Pederson, C., & Kanwar, R. (2018). Salmonella and fecal indicator bacteria survival in soils amended with poultry manure. Water, Air, & Soil Pollution, 229, 1–14. https://doi.org/10.1007/s11270-017-3667-z
Huang, F. Y., Zhou, X. Y., Lin, C., Jin, M. K., Neilson, R., Li, H., & Su, J. Q. (2022). Conurbation size drives antibiotic resistance along the river. Science of the Total Environment, 823, 153822. https://doi.org/10.1016/j.scitotenv.2022.153822
Jang, J., Hur, H. G., Sadowsky, M. J., Byappanahalli, M. N., Yan, T., & Ishii, S. (2017). Environmental Escherichia coli: Ecology and public health implications—a review. Journal of Applied Microbiology, 123(3), 570–581. https://doi.org/10.1111/jam.13468
Jeong, T. Y., & Simpson, M. J. (2019). Daphnia magna metabolic profiling as a promising water quality parameter for the biological early warning system. Water Research, 166, 115033. https://doi.org/10.1016/j.watres.2019.115033
Kadam, A. D., Kishore, G., Mishra, D. K., & Arunachalam, K. (2020). Microalgal diversity as an indicator of the state of the environment of water bodies of Doon valley in Western Himalaya, India. Ecological Indicators, 112, 106077. https://doi.org/10.1016/j.ecolind.2020.106077
Keke, U. N., Mgbemena, A. S., Arimoro, F. O., & Omalu, I. C. (2020). Biomonitoring of effects and accumulations of heavy metals insults using some helminth parasites of fish as bio-indicators in an Afrotropical stream. Frontiers in Environmental Science, 8, 576080. https://doi.org/10.3389/fenvs.2020.576080
Krupińska, M., Antolová, D., Tołkacz, K., Szczepaniak, K., Strachecka, A., Goll, A., Nowicka, J., Baranowicz, K., Bajer, A., Behnke, J. M., & Grzybek, M. (2023). Grassland versus forest dwelling rodents as indicators of environmental contamination with the zoonotic nematode Toxocara spp. Scientific Reports, 13(1), 483. https://doi.org/10.1038/s41598-022-23891-6
Lappan, R., Henry, R., Chown, S. L., Luby, S. P., Higginson, E. E., Bata, L., Jirapanjawat, T., Schang, C., Openshaw, J. J., O’Toole, J., Lin, A., Tela, A., Turagabeci, A., Wong, T. H. F., French, M. A., Brown, R. R., Leder, K., Greening, C., & McCarthy, D. (2021). Monitoring of diverse enteric pathogens across environmental and host reservoirs with TaqMan array cards and standard qPCR: A methodological comparison study. The Lancet Planetary Health, 5(5), e297–e308. https://doi.org/10.1016/S2542-5196(21)00051-6
Leifels, M., Jurzik, L., Wilhelm, M., & Hamza, I. A. (2015). Use of ethidium monoazide and propidium monoazide to determine viral infectivity upon inactivation by heat, UV-exposure and chlorine. International Journal of Hygiene and Environmental Health, 218(8), 686–693. https://doi.org/10.1016/j.ijheh.2015.02.003
Li, C., Quan, Q., Gan, Y., Dong, J., Fang, J., Wang, L., & Liu, J. (2020). Effects of heavy metals on microbial communities in sediments and establishment of bioindicators based on microbial taxa and function for environmental monitoring and management. Science of the Total Environment, 749, 141555. https://doi.org/10.1016/j.scitotenv.2020.141555
Li, X., Qu, C., Bian, Y., Gu, C., Jiang, X., & Song, Y. (2019). New insights into the responses of soil microorganisms to polycyclic aromatic hydrocarbon stress by combining enzyme activity and sequencing analysis with metabolomics. Environmental Pollution, 255, 113312. https://doi.org/10.1016/j.envpol.2019.113312
Li, Y., Chen, H., & Teng, Y. (2020). Source apportionment and source-oriented risk assessment of heavy metals in the sediments of an urban river-lake system. Science of the Total Environment, 737, 140310. https://doi.org/10.1016/j.scitotenv.2020.140310
Li, Y., Zheng, L., Zhang, Y., Liu, H., & Jing, H. (2019). Comparative metagenomics study reveals pollution induced changes of microbial genes in mangrove sediments. Scientific Reports, 9(1), 5739. https://doi.org/10.1038/s41598-019-42260-4
Liang, H., de Haan, W. P., Cerda-Domenech, M., Méndez, J., Lucena, F., García-Aljaro, C., Sanchez-Vidal, A., & Ballesté, E. (2023). Detection of faecal bacteria and antibiotic resistance genes in biofilms attached to plastics from human-impacted coastal areas. Environmental Pollution, 319, 120983. https://doi.org/10.1016/j.envpol.2022.120983
Lin, L., Wang, F., Chen, H., Fang, H., Zhang, T., & Cao, W. (2021). Ecological health assessments of rivers with multiple dams based on the biological integrity of phytoplankton: A case study of North Creek of Jiulong River. Ecological Indicators, 121, 106998. https://doi.org/10.1016/j.ecolind.2020.106998
Lozano, P., Trombini, C., Crespo, E., Blasco, J., & Moreno-Garrido, I. (2014). ROI-scavenging enzyme activities as toxicity biomarkers in three species of marine microalgae exposed to model contaminants (copper, Irgarol and atrazine). Ecotoxicology and Environmental Safety, 104, 294–301. https://doi.org/10.1016/j.ecoenv.2014.03.021
Luo, G., Jin, T., Zhang, H., Peng, J., Zuo, N., Huang, Y., Han, Y., Tian, C., Yang, Y., Peng, K., & Fei, J. (2022). Deciphering the diversity and functions of plastisphere bacterial communities in plastic-mulching croplands of subtropical China. Journal of Hazardous Materials, 422, 126865. https://doi.org/10.1016/j.jhazmat.2021.126865
Lv, B., Cui, Y., Tian, W., Wei, H., Chen, Q., Liu, B., Zhang, D., & Xie, B. (2020). Vessel transport of antibiotic resistance genes across oceans and its implications for ballast water management. Chemosphere, 253, 126697. https://doi.org/10.1016/j.chemosphere.2020.126697
Mahanty, S., Tudu, P., Ghosh, S., Chatterjee, S., Das, P., Bhattacharyya, S., Das, S., Acharya, K., & Chaudhuri, P. (2021). Chemometric study on the biochemical marker of the manglicolous fungi to illustrate its potentiality as a bio indicator for heavy metal pollution in Indian Sundarbans. Marine Pollution Bulletin, 173, 113017. https://doi.org/10.1016/j.marpolbul.2021.113017
Manaia, C. M., Rocha, J., Scaccia, N., Marano, R., Radu, E., Biancullo, F., Cerqueira, F., Fortunato, G., Lakovides, I. C., Zammit, I., Kampouris, I., Vaz-Moreira, I., & Nunes, O. C. (2018). Antibiotic resistance in wastewater treatment plants: Tackling the black box. Environment International, 115, 312–324. https://doi.org/10.1016/j.envint.2018.03.044
Manisalidis, I., Stavropoulou, E., Stavropoulos, A., & Bezirtzoglou, E. (2020). Environmental and health impacts of air pollution: A review. Frontiers in Public Health, 8, 14. https://doi.org/10.3389/fpubh.2020.00014
Mannion, F., Hillary, L. S., Malham, S. K., & Walker, D. I. (2020). Emerging technologies for the rapid detection of enteric viruses in the aquatic environment. Current Opinion in Environmental Science & Health, 16, 1–6. https://doi.org/10.1016/j.coesh.2020.01.007
Mantha, S., Anderson, A., Acharya, S. P., Harwood, V. J., & Weidhaas, J. (2017). Transport and attenuation of Salmonella enterica, fecal indicator bacteria and a poultry litter marker gene are correlated in soil columns. Science of the Total Environment, 598, 204–212. https://doi.org/10.1016/j.scitotenv.2017.04.020
Martin, B. C., Middleton, J. A., Skrzypek, G., Kendrick, G. A., Cosgrove, J., & Fraser, M. W. (2022). Composition of seagrass root associated bacterial communities are linked to nutrients and heavy metal concentrations in an anthropogenically influenced estuary. Frontiers in Marine Science, 8, 768864. https://doi.org/10.3389/fmars.2021.768864
Masachessi, G., Prez, V. E., Michelena, J. F., Lizasoain, A., Ferreyra, L. J., Martinez, L. C., Giordano, M. O., Barril, P. A., Paván, J. V., Pisano, M. B., Farías, A. A., Isa, M. B., Ré, V. E., Colina, R., & Nates, S. V. (2021). Proposal of a pathway for enteric virus groups detection as indicators of faecal contamination to enhance the evaluation of microbiological quality in freshwater in Argentina. Science of the Total Environment, 760, 143400. https://doi.org/10.1016/j.scitotenv.2020.143400
Mays, C., Garza, G. L., Waite-Cusic, J., Radniecki, T. S., & Navab-Daneshmand, T. (2021). Impact of biosolids amendment and wastewater effluent irrigation on enteric antibiotic-resistant bacteria–A greenhouse study. Water Research X, 13, 100119. https://doi.org/10.1016/j.wroa.2021.100119
McEgan, R., Mootian, G., Goodridge, L. D., Schaffner, D. W., & Danyluk, M. D. (2013). Predicting Salmonella populations from biological, chemical, and physical indicators in Florida surface waters. Applied and Environmental Microbiology, 79(13), 4094–4105. https://doi.org/10.1128/AEM.00777-13
McMinn, B. R., Ashbolt, N. J., & Korajkic, A. (2017). Bacteriophages as indicators of faecal pollution and enteric virus removal. Letters in Applied Microbiology, 65(1), 11–26. https://doi.org/10.1111/lam.12736
Mokhtarzadeh, A., Eivazzadeh-Keihan, R., Pashazadeh, P., Hejazi, M., Gharaatifar, N., Hasanzadeh, M., Baradaran, B., & de la Guardia, M. (2017). Nanomaterial-based biosensors for detection of pathogenic virus. TrAC Trends in Analytical Chemistry, 97, 445–457. https://doi.org/10.1016/j.trac.2017.10.005
Montazeri, N., Goettert, D., Achberger, E. C., Johnson, C. N., Prinyawiwatkul, W., & Janes, M. E. (2015). Pathogenic enteric viruses and microbial indicators during secondary treatment of municipal wastewater. Applied and Environmental Microbiology, 81(18), 6436–6445. https://doi.org/10.1128/AEM.01218-15
Niestępski, S., Harnisz, M., Korzeniewska, E., & Osińska, A. (2020). Markers specific to Bacteroides fragilis group bacteria as indicators of anthropogenic pollution of surface waters. International Journal of Environmental Research and Public Health, 17(19), 7137. https://doi.org/10.3390/ijerph17197137
Nováková, A., Hubka, V., Valinová, Š., Kolařík, M., & Hillebrand-Voiculescu, A. M. (2018). Cultivable microscopic fungi from an underground chemosynthesis-based ecosystem: A preliminary study. Folia Microbiologica, 63, 43–55. https://doi.org/10.1007/s12223-017-0527-6
O'Neill, E. A., Rowan, N. J., & Fogarty, A. M. (2019). Novel use of the alga Pseudokirchneriella subcapitata, as an early-warning indicator to identify climate change ambiguity in aquatic environments using freshwater finfish farming as a case study. Science of the Total Environment, 692, 209–218. https://doi.org/10.1016/j.scitotenv.2019.07.243
Palacios, O. A., Adame-Gallegos, J. R., Rivera-Chavira, B. E., & Nevarez-Moorillón, G. V. (2021). Antibiotics, multidrug-resistance bacteria, and antibiotic resistance genes: Indicators of contamination in mangroves? Antibiotics, 10(9), 1103. https://doi.org/10.3390/antibiotics10091103
Palacios, O. A., Contreras, C. A., Muñoz-Castellanos, L. N., González-Rangel, M. O., Rubio-Arias, H., Palacios-Espinosa, A., & Nevárez-Moorillón, G. V. (2017). Monitoring of indicator and multidrug resistant bacteria in agricultural soils under different irrigation patterns. Agricultural Water Management, 184, 19–27. https://doi.org/10.1016/j.agwat.2017.01.001
Parmar, T. K., Rawtani, D., & Agrawal, Y. K. (2016). Bioindicators: The natural indicator of environmental pollution. Frontiers in Life Science, 9(2), 110–118. https://doi.org/10.1080/21553769.2016.1162753
Paruch, L., Paruch, A. M., Eiken, H. G., & Sørheim, R. (2019). Aquatic microbial diversity associated with faecal pollution of Norwegian waterbodies characterized by 16S rRNA gene amplicon deep sequencing. Microbial Biotechnology, 12(6), 1487–1491. https://doi.org/10.1111/1751-7915.13461
Pastorino, P., Broccoli, A., Anselmi, S., Bagolin, E., Prearo, M., Barceló, D., & Renzi, M. (2022). The microalgae Chaetoceros tenuissimus exposed to contaminants of emerging concern: A potential alternative to standardized species for marine quality assessment. Ecological Indicators, 141, 109075. https://doi.org/10.1016/j.ecolind.2022.109075
Pinilla, G. A., Montenegro, L. C., Melgarejo, L. M., Molano-González, N., Pineda, A., Delgadillo, I. P., & Forero, M. A. (2021). Growth rates of microalgae encapsulated in calcium. Limnetica, 40(2), 385–398. https://doi.org/10.23818/limn.40.26
Powers, N. C., Wallgren, H. R., Marbach, S., & Turner, J. W. (2020). Relationship between rainfall, fecal pollution, antimicrobial resistance, and microbial diversity in an urbanized subtropical bay. Applied and Environmental Microbiology, 86(19), e01229–e01220. https://doi.org/10.1128/AEM.01229-20
Prevost, B., Lucas, F. S., Goncalves, A., Richard, F., Moulin, L., & Wurtzer, S. (2015). Large scale survey of enteric viruses in river and waste water underlines the health status of the local population. Environment International, 79, 42–50. https://doi.org/10.1016/j.envint.2015.03.004
Rafailidis, P. I., & Kofteridis, D. (2022). Proposed amendments regarding the definitions of multidrug-resistant and extensively drug-resistant bacteria. Expert Review of Anti-Infective Therapy, 20(2), 139–146. https://doi.org/10.1080/14787210.2021.1945922
Rathnayake, I. V. N., Megharaj, M., & Naidu, R. (2023). Sol–gel immobilized optical microalgal biosensor for monitoring Cd, Cu and Zn bioavailability in freshwater. Bulletin of Environmental Contamination and Toxicology, 110(4), 73. https://doi.org/10.1007/s00128-023-03709-5
Razli, S. A., Abas, A., Ismail, A., Othman, M., Mohtar, A. A. A., Baharudin, N. H., Aiyub, K., & Latif, M. T. (2022). Epiphytic microalgae as biological indicators for carbon monoxide concentrations in different areas of Peninsular Malaysia. Environmental Forensics, 23(3-4), 314–323. https://doi.org/10.1080/15275922.2020.1850560
Reno, U., Regaldo, L., Vidal, E., Mariani, M., Zalazar, C., & Gagneten, A. M. (2016). Water polluted with glyphosate formulations: Effectiveness of a decontamination process using Chlorella vulgaris growing as bioindicator. Journal of Applied Phycology, 28, 2279–2286. https://doi.org/10.1007/s10811-015-0755-6
Rinne, H., Korpinen, S., Mattila, J., & Salovius-Lauren, S. (2018). Functionality of potential macroalgal indicators in the northern Baltic Sea. Aquatic Botany, 149, 52–60. https://doi.org/10.1016/j.aquabot.2018.05.006
Rossi, A., Wolde, B. T., Lee, L. H., & Wu, M. (2020). Prediction of recreational water safety using Escherichia coli as an indicator: Case study of the Passaic and Pompton rivers, New Jersey. Science of the Total Environment, 714, 136814. https://doi.org/10.1016/j.scitotenv.2020.136814
Rothenheber, D., & Jones, S. (2018). Enterococcal concentrations in a coastal ecosystem are a function of fecal source input, environmental conditions, and environmental sources. Applied and Environmental Microbiology, 84(17), e01038–e01018. https://doi.org/10.1128/AEM.01038-18
Rybak, A. S. (2021). Freshwater macroalga, Ulva pilifera (Ulvaceae, Chlorophyta) as an indicator of the trophic state of waters for small water bodies. Ecological Indicators, 121, 106951. https://doi.org/10.1016/j.ecolind.2020.106951
Sanzani, S. M., Li Destri Nicosia, M. G., Faedda, R., Cacciola, S. O., & Schena, L. (2014). Use of quantitative PCR detection methods to study biocontrol agents and phytopathogenic fungi and oomycetes in environmental samples. Journal of Phytopathology, 162(1), 1–13. https://doi.org/10.1111/jph.12147
Saptalena, L. G., Kuklya, A., & Telgheder, U. (2015). Gas chromatography–differential mobility spectrometry and gas chromatography–mass spectrometry for the detection of coliform bacteria. International Journal of Mass Spectrometry, 388, 17–25. https://doi.org/10.1016/j.ijms.2015.07.022
Saxena, G., Bharagava, R. N., Kaithwas, G., & Raj, A. (2015). Microbial indicators, pathogens and methods for their monitoring in water environment. Journal of Water and Health, 13(2), 319–339. https://doi.org/10.2166/wh.2014.275
Sazykina, M. A., Minkina, T. M., Konstantinova, E. Y., Khmelevtsova, L. E., Azhogina, T. N., Antonenko, E. M., Karchava, S. K., Limova, M. V., Sushkova, S. N., Polienko, E. A., Birukova, O. A., Mandzhieva, S. S., Kudeevskaya, E. M., Khammami, M. I., Rakin, A. V., & Sazykin, I. S. (2022). Pollution impact on microbial communities composition in natural and anthropogenically modified soils of Southern Russia. Microbiological Research, 254, 126913. https://doi.org/10.1016/j.micres.2021.126913
Silva, D. M., & Domingues, L. (2015). On the track for an efficient detection of Escherichia coli in water: A review on PCR-based methods. Ecotoxicology and Environmental Safety, 113, 400–411. https://doi.org/10.1016/j.ecoenv.2014.12.015
Suchorab, Z., Frąc, M., Guz, Ł., Oszust, K., Łagód, G., Gryta, A., Bilińska-Wielgus, N., & Czerwiński, J. (2019). A method for early detection and identification of fungal contamination of building materials using e-nose. PLoS One, 14(4), e0215179. https://doi.org/10.1371/journal.pone.0215179
Suzuki, Y., Niina, K., Matsuwaki, T., Nukazawa, K., & Iguchi, A. (2018). Bacterial flora analysis of coliforms in sewage, river water, and ground water using MALDI-TOF mass spectrometry. Journal of Environmental Science and Health, Part A, 53(2), 160–173. https://doi.org/10.1080/10934529.2017.1383128
Tang, C., Yi, Y., Yang, Z., Zhou, Y., Zerizghi, T., Wang, X., Cui, X., & Duan, P. (2019). Planktonic indicators of trophic states for a shallow lake (Baiyangdian Lake, China). Limnologica, 78, 125712. https://doi.org/10.1016/j.limno.2019.125712
Tinoco-Pérez, L. I., Navarrete, K. A. S., Aparicio, I. A. H., Ortega, M. A. H., Mejía, G. C. M., & Mejia, J. C. (2019). Water quality study of the Actopan river in the localities of Santa Rosa and La Linda, Veracruz using macroinvertebrates and diatoms as bioindicators. Journal of Entomology and Zoology Studies, 7(1), 146–150.
Truchado, P., Hernandez, N., Gil, M. I., Ivanek, R., & Allende, A. (2018). Correlation between E. coli levels and the presence of foodborne pathogens in surface irrigation water: Establishment of a sampling program. Water Research, 128, 226–233. https://doi.org/10.1016/j.watres.2017.10.041
Von Söhsten, A. L., da Silva, A. V., & Rubinsky-Elefant, G. (2017). Anti-Toxocara spp. IgY antibodies in poultry sold in street markets from Feira de Santana, Bahia, Northeastern Brazil. Veterinary Parasitology: Regional Studies and Reports, 8, 86–89. https://doi.org/10.1016/j.vprsr.2017.02.006
Wang, L., Zhang, J., Li, H., Yang, H., Peng, C., Peng, Z., & Lu, L. (2018). Shift in the microbial community composition of surface water and sediment along an urban river. Science of the Total Environment, 627, 600–612. https://doi.org/10.1016/j.scitotenv.2018.01.203
Wang, Z., Xiao, G., Zhou, N., Qi, W., Han, L., Ruan, Y., Guo, D., & Zhou, H. (2015). Comparison of two methods for detection of fecal indicator bacteria used in water quality monitoring of the Three Gorges Reservoir. Journal of Environmental Sciences, 38, 42–51. https://doi.org/10.1016/j.jes.2015.04.029
Waso, M., Khan, S., & Khan, W. (2018). Microbial source tracking markers associated with domestic rainwater harvesting systems: Correlation to indicator organisms. Environmental Research, 161, 446–455. https://doi.org/10.1016/j.envres.2017.11.043
Wijaya, J., Byeon, H., Jung, W., Park, J., & Oh, S. (2023). Machine learning modeling using microbiome data reveal microbial indicator for oil-contaminated groundwater. Journal of Water Process Engineering, 53, 103610. https://doi.org/10.1016/j.jwpe.2023.103610
Woodcock, S. H., Meier, S., Keeley, N. B., & Bannister, R. J. (2019). Fate and longevity of terrestrial fatty acids from caged fin-fish aquaculture in dynamic coastal marine systems. Ecological Indicators, 103, 43–54. https://doi.org/10.1016/j.ecolind.2019.03.057
Wu, H., Li, Y., Zhang, W., Wang, C., Wang, P., Niu, L., Du, J., & Gao, Y. (2019). Bacterial community composition and function shift with the aggravation of water quality in a heavily polluted river. Journal of Environmental Management, 237, 433–441. https://doi.org/10.1016/j.jenvman.2019.02.101
Wu, Z., Greaves, J., Arp, L., Stone, D., & Bibby, K. (2020). Comparative fate of CrAssphage with culturable and molecular fecal pollution indicators during activated sludge wastewater treatment. Environment International, 136, 105452. https://doi.org/10.1016/j.envint.2019.105452
Yu, P., Zaleski, A., Li, Q., He, Y., Mapili, K., Pruden, A., Alvarez, P. J. J., & Stadler, L. B. (2018). Elevated levels of pathogenic indicator bacteria and antibiotic resistance genes after Hurricane Harvey’s flooding in Houston. Environmental Science & Technology Letters, 5(8), 481–486. https://doi.org/10.1021/acs.estlett.8b00329
Zachleder, V., Bišová, K., & Vítová, M. (2016). The cell cycle of microalgae. In M. Borowitzka, J. Beardall, & J. Raven (Eds.), The physiology of microalgae. Developments in Applied Phycology (Vol. 6). Springer. https://doi.org/10.1007/978-3-319-24945-2_1
Zampieri, B. D. B., da Costa Andrade, V., Chinellato, R. M., Garcia, C. A. B., de Oliveira, M. A., Brucha, G., & de Oliveira, A. J. F. C. (2020). Heavy metal concentrations in Brazilian port areas and their relationships with microorganisms: Can pollution in these areas change the microbial community? Environmental Monitoring and Assessment, 192, 1–17. https://doi.org/10.1007/s10661-020-08413-z
Zhang, M., Sun, Q., Chen, P., Wei, X., & Wang, B. (2022). How microorganisms tell the truth of potentially toxic elements pollution in environment. Journal of Hazardous Materials, 431, 128456. https://doi.org/10.1016/j.jhazmat.2022.128456
Acknowledgements
Francisco J. Choix acknowledges CONAHCYT (Consejo Nacional de Humanidades, Ciencia y Tecnología, Mexico) for the support under the Program-Project 90 Cátedras CONAHCYT; Diana Fischer for English edition and Itzel Miyuki Choix-Valdez for graphic design.
Author information
Authors and Affiliations
Contributions
Francisco J. Choix and Oskar A. Palacios writing the original draft; Francisco J. Choix, Oskar A. Palacios, and Virginia Guadalupe Nevárez-Moorillón review the final version of manuscript
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Choix, F.J., Palacios, O.A. & Nevarez-Moorillón, G.V. Traditional and new proposals for environmental microbial indicators—a review. Environ Monit Assess 195, 1521 (2023). https://doi.org/10.1007/s10661-023-12150-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-023-12150-4