Microcystis aeruginosa aggravated arsenic accumulation in silver carp.pdf

journal of environmental sciences 146(2024)8190Available online at w w w.e l s e v i e r.c o m/l o c a t e/j e s Research Article Microcystis aeruginosa aggravated arsenic accumulation in silver carp during silver carp controlling algal bloom in arsenic-contaminated water Xinxin Zhao 1,Zuoming Xie 2,Taikun Liu 3,Zuoping Zhao 1,Fengmin Song 1,Zhifeng Liu 1 1 State Key Laboratory of Qinba Bio-Resource and Ecological Environment,School of Chemistry&Environment Science,Shaanxi University of Technology,Hanzhong 723001,China 2 State Key Laboratory of Biogeology and Environmental Geology&School of Environmental Studies,China University of Geosciences,Wuhan 430074,China 3 Linyi Vocational University of Science and Technology,Linyi 276000,China a r t i c l e i n f o Article history:Received 27 March 2023 Revised 30 May 2023 Accepted 1 June 2023 Available online 7 June 2023 Keywords:Microcystis aeruginosa bloom Silver carp Biological control Arsenic transfer Bioaccumulation a b s t r a c t Silver carp mediated biological control techniques are often advocated for controlling cyanobacteria blooms in eutrophic water,which are often enriched with arsenic(As).How-ever,the transfer and fate of As during the biological control of cyanobacteria blooms by silver carp in As-rich eutrophic water remain unclear.Based on the simulated ecosystem experiment,the accumulation of As in silver carp and the transfer and fate of As in the wateralgaesilver carp system during Microcystis aeruginosa blooms controlled by silver carp were investigated.Microcystis aeruginosa showed high tolerance to As(V).The accumulation of As in different tissues of silver carp was different,as follows:intestine liver gill skin muscle.After silver carp ingested As-rich Microcystis aeruginosa,As accumulation in the intestine,liver,gill,and skin of silver carp was enhanced under the action of digestion and skin contact.Compared with the system without algal,As accumulation in the intestine,liver,gill,and skin of silver carp increased by 1.1,3.3,3.3,and 9.6 times,respectively,after incubation for 30 days in the system with Microcystis aeruginosa,while the accumulation of As in the muscle was only slightly increased by 0.56 mg/kg.This work revealed the transfer and fate of As during algal control by silver carp,elucidated the accumulation mechanism of As in water-algae-silver carp system,enriched our understanding of As bioaccumulation and transformation in As-rich eutrophication water,and provided a scientific basis for as-sessing and predicting As migration and enrichment in water-algae-silver carp system.2023 The Research Center for Eco-Environmental Sciences,Chinese Academy of Sciences.Published by Elsevier B.V.Corresponding author.E-mail:(Z.Xie).https:/doi.org/10.1016/j.jes.2023.06.0011001-0742/2023 The Research Center for Eco-Environmental Sciences,Chinese Academy of Sciences.Published by Elsevier B.V.82 journal of environmental sciences 146(2024)8190 Introduction Water eutrophication caused by human activities such as agri-culture and industrial production is one of the world s wa-ter environmental problems.Water eutrophication can pro-mote the frequent outbreak of algal blooms in water bodies(Zhang et al.,2023),which will cause harm on drinking wa-ter sources,industrial and agricultural water,aquaculture and tourism services by producing odor substances and cyanobac-terial toxins,and pose potential threats to aquatic ecological environment and public health(Awual,2019;Dadi et al.,2023).In order to control cyanobacterial blooms,the non-classical biological manipulation theory,namely,to directly control the algal biomass by increasing the number of typical plankton feeding fish such as silver carp,has been successfully ap-plied in the treatment of typical eutrophic water bodies,such as Taihu Lake,Dianchi Lake,Chaohu Lake,and Wuhan East Lake in China(Pivokonsky et al.,2016;Wang et al.,2022).Sil-ver carp has a very wide range of filter feeding,usually op-erating in the upper and middle water bodies.They mainly feed on planktonic algae and are the dominant fish for bi-ological algal control(etlkov et al.,2020;Yi et al.,2016).In addition,the feeding behavior of silver carp enriches the food chain structure in the water body,enhances metabolism among different populations,regulates algae biomass,and also intensifies the conversion rate of nutrients(Wang et al.,2022).Biomanipulation technology can improve the water en-vironment by regulating the ecological function of a trophic level of aquatic community,but it ignores the regulation func-tion of the whole biological chain.In fact,any trophic level in the food chain will be affected by the feeding and com-petition of neighboring trophic levels.In the natural aquatic ecosystem,aquatic organisms such as algae and filter-feeding fish can restrict and affect their biomass through feeding and competition,and also profoundly affect the absorption and migration of pollutants such as nutrients(nitrogen,phospho-rus,etc.)and heavy metal(loid)s in water through biological enrichment and transmission(Magellan et al.,2014).In the prevention and control of eutrophic water by biomanipula-tion technology,previous studies mainly focused on the dy-namic behavior of algal biomass and typical nutrients such as nitrogen and phosphorus in water(He et al.,2022;Paerl et al.,2011).However,the transmission of heavy metal(loid)s in the food chain and their accumulation characteristics in aquatic organisms still need further research.Arsenic(As),a potential hazardous metalloid element,is one of the important pollutants in aquatic ecological environ-ment(Liu et al.,2023;Ubando et al.,2021;Zhao et al.,2022).High concentrations of As have been found simultaneously in eutrophic water bodies such as Taihu Lake in China(Su et al.,2012),posing serious threats to public health.In the As-rich water environment,As in water bodies and sediments can mi-grate to aquatic organisms and amplify along the food chain step by step,which is toxic,bioaccumulative and bioamplify-ing,posing a great threat to food safety and human health.Many lower trophic level aquatic organisms in the water en-vironment,such as bacteria,algae,and aquatic plants,have significant bioaccumulation capacities for As(Rathod et al.,2019;Wang et al.,2013,2024).These As can migrate to higher trophic level aquatic organisms such as invertebrates and fish through the food chain,and eventually transfer to the human body,causing a variety of diseases such as nerve damage,liver necrosis,and skin cancer(Andosch et al.,2015;Banerjee et al.,2023).Recent studies have shown that different algae species have significantly different bioaccumulation abilities for As(Gao et al.,2018;Lin et al.,2020).Previous studies have pointed out that cyanobacteria are one of the largest and most impor-tant prokaryotic autotrophs in aquatic systems(Wang et al.,2013).Microcystis aeruginosa(M.aeruginosa),as the most com-mon cyanobacteria in eutrophic water bodies,can form algal blooms and pose a threat to the aquatic ecological environ-ment(Liu et al.,2023;Tarafdar et al.,2022).In the treatment of eutrophic water based on non-classical biomanipulation technology,the biological control technology of stocking al-gal eating fish such as silver carp is used to control M.aerug-inosa bloom,and the catch is usually collected at the same time to increase economic benefits(Wang et al.,2022;Yi et al.,2016).However,in the As-rich eutrophic water,the accumula-tion characteristics of As in silver carp and the transfer and fate of As in water-algae-silver carp system during the bio-logical control of M.aeruginosa bloom by silver carp are still unclear.In this work,based on the simulated ecosystem experi-ment,the transfer and fate of As in the water-algal-silver carp system during the control of M.aeruginosa by silver carp were investigated.The objectives of this study were as follows:(1)investigating the bioaccumulation of M.aeruginosa to soluble As;(2)revealing the accumulation characteristics of As in sil-ver carp in the As-rich eutrophic water;and(3)explaining the transfer and fate of As in the water-algae-silver carp system.The results were of great significance for predicting As migra-tion and accumulation during the control of M.aeruginosa by silver carp in the As-rich eutrophic water and for assessing their health risks.1.Materials and methods 1.1.M.aeruginosa/silver carp and culture conditions In this study,M.aeruginosa(FACHB-905)was obtained from In-stitute of Hydrology,Chinese Academy of Sciences,China.The algal strain was cultured in BG-11 medium(Singh et al.,2018)under aerobic conditions in a constant temperature light incu-bator at 27 1 C under alight intensity of 2,000 200 Lux with 12 hr bright:12 hr dark.This medium contained the follow-ing components:NaNO3,1500 mg/L;ferric ammenium citrate,6 mg/L;MgSO4 7H2 O,75 mg/L;EDTANa2,1 mg/L;KHPO4 3H2 O,0.04 mg/L;Na2 CO3,2 mg/L;CaCl2 2H2 O,36 mg/L;citric acid,6 mg/L;trace elements solution A5,1 mL/L,pH=7.0.The cul-ture flask was shaken three times a day manually to increase the amount of dissolved CO2 in the culture system and to pro-vide carbon source for the growth of algae.Silver carp were obtained from Institute of Hydroecology,Ministry of Water Resources&Chinese Academy of Sciences,China.The silver carp was of the same variety and size,with a body weight of 76.6 1.7 g and a body length of 17.2 1.5 cm.These fish were physically unharmed and healthy.Be-fore the experiment,silver carp were cultured in an aquarium journal of environmental sciences 146(2024)819083(80 cm in length,45 cm in width,and 45 cm in height)in the laboratory and acclimated to the laboratory environment by feeding M.aeruginosa for 30 days.The life activity of silver carp was normal and the mortality rate was less than 3%.The cul-ture water was fully aerated tap water for 24 hr.The water temperature was maintained at 26.5 0.5 C,the dissolved oxygen was greater than 6.9 mg/L,the pH value was 7.0 0.1,with 12 hr bright:12 hr dark.1.2.Enrichment of M.aeruginosa for As A series of 250 mL Erlenmeyer flasks were used as bioreactors,and 200 mL of BG11 medium containing different As(V)con-centrations(0,5,200,and 1,000 g/L)was added to each flask.Under sterile conditions,M.aeruginosa cells in logarithmic growth phase were centrifuged and concentrated(5,000 rpm,10 min)(He et al.,2021),and then centrifuged and cleaned three times with sterile deionized water to remove the extra-cellular culture solution.The algal cells were inoculated into each reaction flask with an initial optical density of about 0.2.After that,they were incubated in a light incubator at 27 1 C under alight intensity of 2,000 200 Lux with 12 hr bright:12 hr dark.Three parallel experiments were set for each experi-mental group.Each flask was manually shaken 3-4 times a day and incubated for 12 days.Samples were taken regularly to de-termine the changes of algae density,carotenoid,and chloro-phyll a content.M.aeruginosa cells in logarithmic growth phase(approxi-mately 1 106 cells/mL)were inoculated into the flasks with the solution containing As(V)(200 g/L),pH 7.0,and inoculated for 24 hr.All experiments were set in three parallel.During the whole experiment,the biomass of M.aeruginosa in each sys-tem did not change significantly(Appendix A Fig.S1).Samples were taken regularly,and the supernatant was collected after centrifugation for 10 min with a centrifuge at 5000 r/min to determine the change of As content in the supernatant.The amount of As adsorbed per unit weight of M.aeruginosa cells was calculated as follows:Qt=V(C0 Ct)m(1)where Qt(g/g)is the amount of As adsorbed by M.aeruginosa cells per unit weight at the sampling time;C0(g/L)is the to-tal As concentration in the initial working solutions;Ct(g/L)is the total As concentration in the solutions at the sampling time;V(L)is the volume of solution;and m(g)is the mass of M.aeruginosa.The As(V)adsorption kinetics of M.aeruginosa cells were fitted by pseudo-first order Eq.(2)and pseudo-second order Eq.(3)models,as follows:Qt=Qe?1 ek1 t?(2)Qt=Q2 e k2 t/(1+Qe k2 t)(3)where Qe(g/g)is the amount of As adsorbed by M.aerugi-nosa cells per unit weight at equilibrium;and k1(min1)and k2(g/g/min)are the adsorption rate constants of the kinetic model,respectively.The content of physically adsorbed,chemically adsorbed,biological adsorbed,and residual As in algal cells was deter-mined based on the previous extraction step for various As speciation(Deng et al.,2006;He et al.,2014),as detailed be-low.After 24 hr,50 mL of sample suspension was removed from each reaction flask and centrifuged at 5,000 r/min for 10 min to collect algal cells;added 10 mL distilled water to the collected algal cells,after shaking at 26 C for 20 min and centrifuging at 5000 r/min for 10 min,the concentration of As in the supernatant was determined,which was the physi-cal adsorption amount of As(mg/g)by M.aeruginosa cells.Af-ter the physically adsorbed As was extracted,the algal cells were collected and washed with 10 mL of 20 mmol/L EDTA-2Na for 10 min;after centrifugation at 5,000 r/min for 10 min,the concentration of As in the supernatant was determined,which was the content of chemically adsorbed As(mg/g)ex-changed by the algal cells.After the chemically adsorbed As was extracted,the algal cells were collected,weighed,and all transferred to the polytetrafluoroethylene digestion tube for digestion;the content of As in the digestion solution was de-termined as the bioabsorption amount of M.aeruginosa cells(mg/g).The residual amount of As in algal cells(mg/g)was the difference between the total amount of As enrichment and the physical,chemical,and biological adsorption amount,in-dicating the content of firmly bound As.1.3.Arsenic accumulation and transfer in silver carp Based on the simulated ecosystem experiment,the simulation study of silver carp controlling cyanobacteria bloom was car-ried out as follows.About 100 L tap water was injected into the glass aquarium and the chlorine was removed by aeration.Be-fore the experiment,all silver carp were domesticated under laboratory conditions for half a month.In the experimental group,30 silver carp were put into the system with As(V)con-centration of 200 g/L,the addition amount of M.aeruginosa was 0.1 g fresh weight/fish and the feed for silver carp was 0.1 g/fish every day.In the control group,30 silver carp were fed 0.1 g/fish of feed daily with As(V)concentration of 200 g/L without M.aeruginosa.During the experiment,the water was changed every 2 days with 80 L of water,and the concentra-tion of As(V)in the system was maintained at 200 g/L.At the same time,strip fish feces were collected by siphon and filter,and impurities in water were cleaned.During the 30-day incu-bation,three silver carp were randomly sampled every 5 days to analyze the change of As content.Bioconcentration factor(BCF)is the ratio between the con-centration of an element in an organism and the background concentrat