Abstract
This study investigated the effects of different types of saline stress on the availability of cadmium (Cd) and bacterial growth. Changes in soil physicochemical properties and DTPA-Cd content as well as microbial responses after the addition of salts were measured. The addition of 18 g kg−1 of salts with NaCl and Na2SO4 increased the available Cd content by up to 17.80%–29.79%. Respiration rate, biomass, and relative bacterial growth decreased with increasing salt concentrations. Estimated salinity tolerance of bacterial communities based on pollution-induced community tolerance. The salinity tolerance index EC50 of the bacterial community was estimated by logistic equation and ranged from 4.32–12.63 g kg−1. Structural equation modeling showed that soil salinity stress significantly affected Cd availability and bacterial community, while bacterial growth characteristics also contributed to reducing available Cd. We conclude that saline stress can alter soil Cd availability in soils by affecting the growth characteristics of soil bacterial communities.
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References
Acosta JA, Faz A, Martínez-Martínez S et al (2011) Enrichment of metals in soils subjected to different land uses in a typical Mediterranean environment (Murcia City, southeast Spain). Appl Geochem 26:405–414. https://doi.org/10.1016/j.apgeochem.2011.01.023
Anderson J, Domsch K (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221. https://doi.org/10.1016/0038-0717(78)90099-8
Aydin ME, Aydin S, Beduk F, Tor A, Tekinay A, Kolb M, Bahadir M (2015) Effects of long-term irrigation with untreated municipal wastewater on soil properties and crop quality. Environ Sci Pollut Res 22:19203–19212. https://doi.org/10.1007/s11356-015-5123-1
Azadi N, Raiesi F (2021) Salinization depresses soil enzyme activity in metal-polluted soils through increases in metal mobilization and decreases in microbial biomass. Ecotoxicology 30:1071–1083. https://doi.org/10.1007/s10646-021-02433-2
Bååth E (1994) Thymidine and leucine incorporation in soil bacteria with different cell-size. Microb Ecol 27:267–278. https://doi.org/10.1007/bf00182410
Bååth E, Pettersson M, Söderberg KH (2001) Adaptation of a rapid and economical microcentrifugation method to measure thymidine and leucine incorporation by soil bacteria. Soil Biol Biochem 33:1571–1574. https://doi.org/10.1016/S0038-0717(01)00073-6
Badran RA (1994) Cellulolytic activity of some cellulose decomposing fungi in salinized soils. Acta Mycol 29:245–251. https://doi.org/10.1007/bf02876599
Becerra-Castro C, Lopes AR, Vaz-Moreira I et al (2015) Wastewater reuse in irrigation: a microbiological perspective on implications in soil fertility and human and environmental health. Environ Int 75:117–135. https://doi.org/10.1016/j.envint.2014.11.001
Bhattacharya S (2020) The role of probiotics in the amelioration of cadmium toxicity. Biol Trace Elem Res 197:440–444. https://doi.org/10.1007/s12011-020-02025-x
Blanck H (2002) A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in Biotic Communities. Hum Ecol Risk Assess 8:1003–1034. https://doi.org/10.1080/1080-700291905792
Boyrahmadi M, Raiesi F (2018) Plant roots and species moderate the salinity effect on microbial respiration, biomass, and enzyme activities in a sandy clay soil. Biol Fertil Soils 54:509–521. https://doi.org/10.1007/s00374-018-1277-6
Choquet CG, Kamekura M, Kushner DJ (1989) In vitro protein-synthesis by the moderate halophile Vibrio costicola-site of action of Cl- ions. J Bacteriol 171:880–886. https://doi.org/10.1128/jb.171.2.880-886.1989
Cruz-Paredes C, Wallander H, Kjøller R, Rousk J (2017) Using community trait-distributions to assign microbial responses to pH changes and cd in forest soils treated with wood ash. Soil Biol Biochem 112:153–164. https://doi.org/10.1016/j.soilbio.2017.05.004
Delgado-Baquerizo M, Oliverio AM, Brewer TE et al (2018) A global atlas of the dominant bacteria found in soil. Science 359:320. https://doi.org/10.1126/science.aap9516
Egamberdieva D, Renella G, Wirth S et al (2010) Secondary salinity effects on soil microbial biomass. Biol Fertil Soils 46:445–449. https://doi.org/10.1007/s00374-010-0452-1
Elizabeth SG, Valencia-Becerril I, Valenzuela-Encinas C et al (2016) Deforestation and cultivation with maize (Zea mays L.) has a profound effect on the bacterial community structure in soil. Land Degrad Dev 27:1122–1130. https://doi.org/10.1002/ldr.2328
Elmajdoub B, Marschner P (2013) Salinity reduces the ability of soil microbes to utilise cellulose. Biol Fertil Soils 49:379–386. https://doi.org/10.1007/s00374-012-0734-x
Elsheikh E, Wood M (1989) Response of chickpea and soybean rhizobia to salt osmotic and specific ion effects of salts. Soil Biol Biochem 21:889–895. https://doi.org/10.1016/0038-0717(89)90077-1
Filipović L, Romić M, Romić D et al (2018) Organic matter and salinity modify cadmium soil (phyto)availability. Ecotoxicol Environ Saf 147:824–831. https://doi.org/10.1016/j.ecoenv.2017.09.041
Gdbrijel O, Davor R, Zed R, Marija R, Monika Z (2009) Cadmium accumulation by muskmelon under salt stress in contaminated organic soil. Sci Total Environ 407:2175–2182. https://doi.org/10.1016/j.scitotenv.2008.12.032
Ghallab A, Usman A (2007) Effect of sodium chloride-induced salinity on phytoavailability and speciation of Cd in soil solution. Water Air Soil Pollut 185:43–51. https://doi.org/10.1007/s11270-007-9424-y
Haj-Amor Z, Hashemi H, Bouri S (2017) Soil salinization and critical shallow groundwater depth under saline irrigation condition in a Saharan irrigated land. Arab J Geosci 10:301. https://doi.org/10.1007/s12517-017-3093-y
Hale B, Evans L, Lambert R (2012) Effects of cement or lime on Cd Co, Cu, Ni, Pb, Sb and Zn mobility in field-contaminated and aged soils. J Hazard Mater 199:119–127. https://doi.org/10.1016/j.jhazmat.2011.10.065
Hou D, Wang R, Gao X et al (2018) Cultivar-specific response of bacterial community to cadmium contamination in the rhizosphere of rice (Oryza sativa L.). Environ Pollut 241:63–73. https://doi.org/10.1016/j.envpol.2018.04.121
Kamble PN, Gaikwad VB, Kuchekar SR, Bååth E (2014) Microbial growth, biomass, community structure and nutrient limitation in high pH and salinity soils from Pravaranagar (India). Eur J Soil Biol 65:87–95. https://doi.org/10.1016/j.ejsobi.2014.10.005
Kaur A, Pan M, Meislin M, Facciotti MT, El-Gewely R, Baliga NS (2006) A systems view of haloarchaeal strategies to withstand stress from transition metals. Genome Res 16:841–854. https://doi.org/10.1101/gr.5189606
Kirchman DL, Knees E, Hodson R (1985) Leucine incorporation and its potential as a measure of protein-synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49:599–607. https://doi.org/10.1128/aem.49.3.599-607.1985
Kubier A, Wilkin RT, Pichler T (2019) Cadmium in soils and groundwater: a review. Appl Geochem. https://doi.org/10.1016/j.apgeochem.2019.104388
Kumar DA, Subrahmanyam G, Mondal R et al (2021) Bio-remediation approaches for alleviation of cadmium contamination in natural resources. Chemosphere. https://doi.org/10.1016/j.chemosphere.2020.128855
Kunhikrishnan A, Bolan NS, Müller K et al (2012) The influence of wastewater irrigation on the transformation and bioavailability of heavy metal (loid)s in soil. Adv Agron 115(21):215–297. https://doi.org/10.1016/B978-0-12-394276-0.00005-6
Liu LZ, Gong Z, Zhang Y et al (2014) Growth, cadmium uptake and accumulation of maize (Zea mays L..) under the effects of arbuscular mycorrhizal fungi. Ecotoxicology 23:1979–1986. https://doi.org/10.1007/s10646-014-1331-6
López-Chuken UJ, López-Domínguez U, Parra-Saldivar R et al (2012) Implications of chloride-enhanced cadmium uptake in saline agriculture: modeling cadmium uptake by maize and tobacco. Int J Environ Sci Technol 9:69–77. https://doi.org/10.1007/s13762-011-0018-2
Ma SC, Zhang HB, Ma ST et al (2015) Effects of mine wastewater irrigation on activities of soil enzymes and physiological properties, heavy metal uptake and grain yield in winter wheat. Ecotoxicol Environ Saf 113:483–490. https://doi.org/10.1016/j.ecoenv.2014.12.031
Malandrino MC, Swarup A, Wanjari RH et al (2011) Accumulation of heavy metals from contaminated soil to plants and evaluation of soil remediation by vermiculite. Chemosphere 82:169–178. https://doi.org/10.1016/j.chemosphere.2010.10.028
Martin H (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35:87–123. https://doi.org/10.1111/j.1574-6976.2010.00234.x
Mavi MS (2017) Impact of salinity on respiration and organic matter dynamics in soils is more closely related to osmotic potential than to electrical conductivity. Pedosphere 27:949–956. https://doi.org/10.1016/s1002-0160(17)60418-1
Mugwar AJ, Harbottle MJ (2016) Toxicity effects on metal sequestration by microbially-induced carbonate precipitation. J Hazard Mater 314:237–248. https://doi.org/10.1016/j.jhazmat.2016.04.039
Poli A, Salerno A, Laezza G, Donato DP, Dumontet S, Nicolaus B (2009) Heavy metal resistance of some thermophiles: potential use of alpha-amylase from Anoxybacillus amylolyticus as a microbial enzymatic bioassay. Res Microbiol 160:99–106. https://doi.org/10.1016/j.resmic.2008.10.012
Rahman M, Hagare D, Maheshwari B et al (2015) Impacts of prolonged drought on salt accumulation in the root zone due to recycled water irrigation. Water Air Soil Pollut 226:90.1-90.18. https://doi.org/10.1007/s11270-015-2370-1
Raiesi F, Sadeghi E (2019) Interactive effect of salinity and cadmium toxicity on soil microbial properties and enzyme activities. Ecotoxicol Environ Saf 168:221–229. https://doi.org/10.1016/j.ecoenv.2018.10.079
Raiesi F, Razmkhah M, Kiani S (2018) Salinity stress accelerates the effect of cadmium toxicity on soil N dynamics and cycling: does joint effect of these stresses matter? Ecotoxicol Environ Saf 153:160–167. https://doi.org/10.1016/j.ecoenv.2018.01.035
Ramakrishna DM, Viraraghavan T (2005) Environmental impact of chemical deicers-A review. Water Air Soil Pollut 166:49–63. https://doi.org/10.1016/j.ecoenv.2018.10.079
Rath KM, Rousk J (2015) Salt effects on the soil microbial decomposer community and their role in organic carbon cycling: a review. Soil Biol Biochem 81:108–123. https://doi.org/10.1016/j.soilbio.2014.11.001
Rath KM, Maheshwari A, Bengtson P, Rousk K (2016) Comparative toxicities of salts on microbial processes in soil. Appl Environ Microbiol Microbiol 82:2012–2020. https://doi.org/10.1128/aem.04052-15
Renella G, Mench M, Landi L, Nannipieri P (2005) Microbial activity and hydrolase synthesis in long-term Cd-contaminated soils. Soil Biol Biochem 37:133–139. https://doi.org/10.1016/j.soilbio.2004.06.015
Rietz DN, Haynes RJ (2003) Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biol Biochem 35:845–854. https://doi.org/10.1016/S0038-0717(03)00125-1
Rosenfeld CE, Chaney RL, Martínez CE (2017) Soil geochemical factors regulate Cd accumulation by metal hyperaccumulating Noccaea caerulescens (J. Presl & C. Presl) F.K. Mey in field-contaminated soils. Sci Total Environ 616–617:279–287. https://doi.org/10.1016/j.scitotenv.2017.11.016
Rousk J, Elyaagubi FK, Jones DL, Godbold DL et al (2011) Bacterial salt tolerance is unrelated to soil salinity across an arid agroecosystem salinity gradient. Soil Biol Biochem 43:1881–1887. https://doi.org/10.1016/j.soilbio.2011.05.007
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. https://doi.org/10.1890/06-0219
Singh K (2016) Microbial and enzyme activities of saline and sodic soils. Land Degrad Dev 27:706–718. https://doi.org/10.1002/ldr.2385
Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils-methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395. https://doi.org/10.1016/j.soilbio.2010.05.007
Suzuki N, Rivero RM, Shulaev V et al (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43. https://doi.org/10.1111/nph.12797
Vodyanitskii YN, Plekhanova IO (2014) Biogeochemistry of heavy metals in contaminated excessively moistened soils (Analytical review). Eurasian Soil Sci 47:153–161. https://doi.org/10.1134/S1064229314030090
Wang T, Liu W, Xiong L et al (2013) Influence of pH, ionic strength and humic acid on competitive adsorption of Pb(II), Cd(II) and Cr(III) onto titanate nanotubes. Chem Eng J 215–216:366–374. https://doi.org/10.1016/j.cej.2012.11.029
Wang J, Wang PM, Gu Y et al (2019a) Iron-manganese (oxyhydro) oxides, rather than oxidation of sulfides, determine mobilization of cd during soil drainage in paddy soil systems. Environ Sci Technol 53:2500–2508. https://doi.org/10.1021/acs.est.8b06863
Wang M, Chen SB, Han Y et al (2019b) Responses of soil aggregates and bacterial communities to soil-Pb immobilization induced by biofertilizer. Chemosphere 220:828–836. https://doi.org/10.1016/j.chemosphere.2018.12.214
Wang M, Li SS, Chen SB et al (2019c) Manipulation of the rhizosphere bacterial community by biofertilizers is associated with mitigation of cadmium phytotoxicity. Sci Total Environ 649:413–421. https://doi.org/10.1016/j.scitotenv.2018.08.174
Wang KC, Xu J, Li YW et al (2020) Response of soil respiration and microbial biomass to soil salinity under different water content in the coastal areas of eastern China. Eurasian Soil Sci 53:82–89. https://doi.org/10.1134/S1064229320010159
Wang M, Zhao SW, Wang LF et al (2021a) Salt stress-induced changes in microbial community structures and metabolic processes result in increased soil cadmium availability. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2021.147125
Wang ZG, Bing HJ, Zhu H et al (2021b) Fractions, contamination and health risk of cadmium in alpine soils on the Gongga Mountain, eastern Tibetan plateau. Bull Environ Contam Toxicol 106:86–91. https://doi.org/10.1007/s00128-020-03073-8
Wessel WW, Tietema A (1992) Calculating gross N transformation rates of 15N pool dilution experiments with acid forest litter analytical and numerical approaches. Soil Biol Biochem 24:931–942. https://doi.org/10.1016/0038-0717(92)90020-X
Wong VNL, Dalal RC, Greene RSB (2008) Salinity and sodicity effects on respiration and microbial biomass of soil. Biol Fertil Soils 44:943–953. https://doi.org/10.1007/s00374-008-0279-1
Wu Y, Song Q, Wu J et al (2021) Field study on the soil bacterial associations to combined contamination with heavy metals and organic contaminants. Sci Total Environ 778:146–282. https://doi.org/10.1016/j.scitotenv.2021.146282
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This work was funded by the National Key Research and Development Program of China (2020YFC1806300-04) and Fundamental Research Funds for Central Non-profit Scientific Institution (1610132021008).
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Wang, L., Qin, L., Sun, X. et al. Linking Bacterial Growth Responses to Soil Salinity with Cd Availability. Bull Environ Contam Toxicol 109, 286–297 (2022). https://doi.org/10.1007/s00128-022-03515-5
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DOI: https://doi.org/10.1007/s00128-022-03515-5