Short-term continuous and pulse Pb exposure causes negative effects on skin histomorphological structure and bacterial composition of adult Pelophylax nigromaculatus
Tóm tắt
Lead (Pb) is a toxic heavy metal often present in the environment as a pulse in water. Traditional toxicity tests are usually carried out under conditions of continuous concentration, without considering the impact of pulse exposure on aquatic organisms. This study aimed to evaluate the effects of short-term continuous and pulse Pb exposures on the skin bacteria and histomorphological structure of Pelophylax nigromaculatus. Results showed that compared to the control (CON) and Pb continuous exposure group (CEPb), the Pb pulse exposure group (PEPb) showed the smallest size of granular glands, which would interfere with the permeability and secretory function of skin, making the individual more sensitive to external pollution. Lead exposure significantly changed the composition and diversity of skin bacteria. Compared to the CON and CEPb groups, the PEPb group showed a significant increase in the abundance of harmful bacteria (e.g., Bacteroidetes and Chryseobacterium) and a decrease in the abundance of beneficial bacteria (e.g., Pseudomonas). PICRUSt software showed that there were differences in the metabolic pathway of skin bacteria among the three groups (CON, CEPb, and PEPb). Overall, this study indicates that Pb pulse exposure can aggravate the toxicity of Pb for frog skin, providing a new framework for simulating short-term heavy metal exposure in the context of frog health.
Tài liệu tham khảo
citation_journal_title=Chemosphere; citation_title=Actinobacteria: Current research and perspectives for bioremediation of pesticides and heavy metals; citation_author=A Alvarez, JM Saez, JS Davila Costa, VL Colin, MS Fuentes, SA Cuozzo, CS Benimeli, MA Polti, MJ Amoroso; citation_volume=166; citation_publication_date=2017; citation_pages=41-62; citation_doi=10.1016/j.chemosphere.2016.09.070; citation_id=CR1
citation_journal_title=Vet Rec; citation_title=Small animal disease surveillance: pruritus and Pseudomonas skin infections; citation_author=E Arsevska, DA Singleton, C Jewell, S Paterson, PH Jones, S Smyth, B Brant, S Dawson, P Noble, F Sánchez-Vizcaíno, AD Radford; citation_volume=183; citation_issue=6; citation_publication_date=2018; citation_pages=182-187; citation_doi=10.1136/vr.k3462; citation_id=CR2
citation_journal_title=J Hazard Mater; citation_title=Probiotics and gut microbiome—prospects and challenges in remediating heavy metal toxicity; citation_author=KB Arun, A Madhavan, R Sindhu, S Emmanual, P Binod, A Pugazhendhi, R Sirohi, R Reshmy, MK Awasthi, E Gnansounou, A Pandey; citation_volume=420; citation_publication_date=2021; citation_pages=126676; citation_doi=10.1016/j.jhazmat.2021.126676; citation_id=CR3
citation_journal_title=Indian J Microbiol; citation_title=Antibacterial, anticancer and neuroprotective activities of rare Actinobacteria from mangrove forest soils; citation_author=AS Azman, I Othman, CM Fang, KG Chan, BH Goh, LH Lee; citation_volume=57; citation_issue=2; citation_publication_date=2017; citation_pages=177-187; citation_doi=10.1007/s12088-016-0627-z; citation_id=CR4
citation_journal_title=Environ Microbiol; citation_title=Assembly of the amphibian microbiome is influenced by the effects of land-use change on environmental reservoirs; citation_author=EM Barnes, S Kutos, N Naghshineh, M Mesko, Q You, JD Lewis; citation_volume=23; citation_issue=8; citation_publication_date=2021; citation_pages=4595-4611; citation_doi=10.1111/1462-2920.15653; citation_id=CR5
citation_journal_title=Mol Ecol; citation_title=Phylogenetic distribution of symbiotic bacteria from Panamanian amphibians that inhibit growth of the lethal fungal pathogen Batrachochytrium dendrobatidis; citation_author=MH Becker, JB Walke, L Murrill, DC Woodhams, LK Reinert, LA Rollins-Smith, EA Burzynski, TP Umile, KPC Minbiole, LK Belden; citation_volume=24; citation_publication_date=2015; citation_pages=1628-1641; citation_doi=10.1111/mec.13135; citation_id=CR6
citation_journal_title=Environ Toxicol Chem; citation_title=Postexposure effects of brief cadmium, zinc, and phenol exposures on freshwater organisms; citation_author=RN Brent, EE Herricks; citation_volume=17; citation_publication_date=1998; citation_pages=2091-2099; citation_doi=10.1002/etc.5620171027; citation_id=CR7
citation_journal_title=BMC Pharmacol Toxicol; citation_title=Ecotoxicology inside the gut: impact of heavy metals on the mouse microbiome; citation_author=J Breton, S Massart, P Vandamme, E Brandt, B Pot, B Foligné; citation_volume=14; citation_issue=1; citation_publication_date=2013; citation_pages=1-11; citation_doi=10.1186/2050-6511-14-62; citation_id=CR8
citation_journal_title=Homeopathy: J Fac Homeopathy; citation_title=Hormesis: principles and applications; citation_author=EJ Calabrese; citation_volume=104; citation_issue=2; citation_publication_date=2015; citation_pages=69-82; citation_doi=10.1016/j.homp.2015.02.007; citation_id=CR9
citation_journal_title=Environ Toxicol Chem; citation_title=Sublethal effects of lead on northern leopard frog (Rana pipiens) tadpoles; citation_author=TH Chen, JA Gross, WH Karasov; citation_volume=25; citation_issue=5; citation_publication_date=2006; citation_pages=1383-1389; citation_doi=10.1897/05-356r.1; citation_id=CR10
citation_journal_title=Sci Total Environ; citation_title=Lead exposure assessment from study near a lead-acid battery factory in China; citation_author=L Chen, Z Xu, M Liu, Y Huang, R Fan, Y Su, G Hu, X Peng, X Peng; citation_volume=429; citation_publication_date=2012; citation_pages=191-198; citation_doi=10.1016/j.scitotenv.2012.04.015; citation_id=CR11
citation_journal_title=J Microbiol; citation_title=Clinical and epidemiological features of Chryseobacterium indologenes infections: analysis of 215 cases; citation_author=FL Chen, GC Wang, SO Teng, TY Ou, FL Yu, WS Lee; citation_volume=46; citation_issue=6; citation_publication_date=2013; citation_pages=425-432; citation_doi=10.1016/j.jmii.2012.08.007; citation_id=CR12
citation_journal_title=Environ Sci Technol; citation_title=Dysregulation of intestinal health by environmental pollutants: involvement of the estrogen receptor and aryl hydrocarbon receptor; citation_author=L Chen, W Zhang, J Hua, C Hu, N Lok-Shun Lai, PY Qian, P Lam, J Lam, B Zhou; citation_volume=52; citation_issue=4; citation_publication_date=2018; citation_pages=2323-2330; citation_doi=10.1021/acs.est.7b06322; citation_id=CR13
citation_journal_title=Chemosphere; citation_title=Predicting the survival of zebrafish larvae exposed to fluctuating pulses of lead and cadmium; citation_author=M Chen, Y Gao, X Bian, J Feng, W Ma, L Zhu; citation_volume=223; citation_publication_date=2019; citation_pages=599-607; citation_doi=10.1016/j.chemosphere.2019.02.102; citation_id=CR14
citation_journal_title=J Vet Med Sci; citation_title=Riemerella anatipestifer infection in domestic ducks in Japan, 2014; citation_author=T Chikuba, H Uehara, S Fumikura, K Takahashi, Y Suzuki, K Hoshinoo, Y Yamamoto; citation_volume=78; citation_issue=10; citation_publication_date=2016; citation_pages=1635-1638; citation_doi=10.1292/jvms.16-0278; citation_id=CR15
citation_journal_title=Sci Total Environ; citation_title=Diversity of cutaneous microbiome of Pelophylax perezi populations inhabiting different environments; citation_author=S Costa, I Lopes, DN Proença, R Ribeiro, PV Morais; citation_volume=572; citation_publication_date=2016; citation_pages=995-1004; citation_doi=10.1016/j.scitotenv.2016.07.230; citation_id=CR16
citation_journal_title=PLoS ONE; citation_title=Cool temperatures reduce antifungal activity of symbiotic bacteria of threatened amphibians–implications for disease management and patterns of decline; citation_author=JH Daskin, SC Bell, L Schwarzkopf, RA Alford; citation_volume=9; citation_issue=6; citation_publication_date=2014; citation_pages=e100378; citation_doi=10.1371/journal.pone.0100378; citation_id=CR17
citation_journal_title=Herpetol J; citation_title=Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians; citation_author=P Daszak, A Strieby, AA Cunningham, JE Longcore, D Porter; citation_volume=24; citation_issue=4; citation_publication_date=2004; citation_pages=23-28; citation_doi=10.1234/ct.v24i4; citation_id=CR18
citation_journal_title=Environ Pollut Res Int; citation_title=Toxicity of atrazine, glyphosate, and quinclorac in bullfrog tadpoles exposed to concentrations below legal limits; citation_author=MF Dornelles, GT Oliveira; citation_volume=23; citation_publication_date=2016; citation_pages=1610-1620; citation_doi=10.1007/s11356-015-5388-4; citation_id=CR19
citation_journal_title=Bull Environ Contam Toxicol; citation_title=Effect of lead exposure on jumping ability in Pelophylax nigromaculata; citation_author=R Duan, M Huang, M Yi, Q Zhao, Y Wan, Y Liu; citation_volume=106; citation_issue=4; citation_publication_date=2021; citation_pages=652-657; citation_doi=10.1007/s00128-021-03150-6; citation_id=CR20
citation_journal_title=Front Public Health; citation_title=Microbiome-aware ecotoxicology of organisms: relevance, pitfalls, and challenges; citation_author=S Duperron, S Halary, A Gallet, B Marie; citation_volume=8; citation_publication_date=2020; citation_pages=407; citation_doi=10.3389/fpubh.2020.00407; citation_id=CR21
citation_journal_title=Environ Int; citation_title=Urinary lead concentration and composition of the adult gut microbiota in a cross-sectional population-based sample; citation_author=S Eggers, N Safdar, AK Sethi, G Suen, PE Peppard, AE Kates, JH Skarlupka, M Kanarek, KMC Malecki; citation_volume=133; citation_publication_date=2019; citation_pages=105122; citation_doi=10.1016/j.envint.2019.105122; citation_id=CR22
citation_journal_title=Appl Soil Ecol; citation_title=Pb, Cd, and Zn soil contamination: monitoring functional and structural impacts on the microbiome; citation_author=C Fajardo, G Costa, M Nande, P Botías, J García-Cantalejo, M Martín; citation_volume=135; citation_publication_date=2019; citation_pages=56-64; citation_doi=10.1016/j.apsoil.2018.10.022; citation_id=CR23
citation_journal_title=Chem Res Toxicol; citation_title=Multi-omics reveals that lead exposure disturbs gut microbiome development, key metabolites, and metabolic pathways; citation_author=B Gao, L Chi, R Mahbub, X Bian, P Tu, H Ru, K Lu; citation_volume=30; citation_publication_date=2017; citation_pages=996-1005; citation_doi=10.1021/acs.chemrestox.6b00401; citation_id=CR24
citation_journal_title=Sci Total Environ; citation_title=Bioaccumulation of trace elements affects chick body condition and gut microbiome in greater flamingos; citation_author=MA Gillingham, F Borghesi, BK Montero, F Migani, A Béchet, M Rendón-Martos, JA Amat, E Dinelli, S Sommer; citation_volume=761; citation_publication_date=2021; citation_pages=143250; citation_doi=10.1016/j.scitotenv.2020.143250; citation_id=CR25
citation_journal_title=China Environ Sci Technol; citation_title=Spatiotemporal trends of heavy metals in indo-pacific humpback dolphins (Sousa chinensis) from the western pearl river estuary; citation_author=D Gui, RQ Yu, L Karczmarski, Y Ding, H Zhang, Y Sun, M Zhang, Y Wu; citation_volume=51; citation_issue=3; citation_publication_date=2017; citation_pages=1848-1858; citation_doi=10.1021/acs.est.6b05566; citation_id=CR26
citation_journal_title=EcoHealth; citation_title=Amphibian pathogen batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species; citation_author=RN Harris, TY James, A Lauer, MA Simon, A Patel; citation_volume=3; citation_issue=1; citation_publication_date=2006; citation_pages=53-56; citation_doi=10.1007/s10393-005-0009-1; citation_id=CR27
citation_journal_title=Biol Rev Camb Philos Soc; citation_title=From frog integument to human skin: dermatological perspectives from frog skin biology; citation_author=IS Haslam, EW Roubos, ML Mangoni, K Yoshizato, H Vaudry, JE Kloepper, DM Pattwell, PF Maderson, R Paus; citation_volume=89; citation_publication_date=2014; citation_pages=618-655; citation_doi=10.1111/brv.12072; citation_id=CR28
citation_journal_title=Environ Toxicol Chem; citation_title=Toxicity of magnesium pulses to tropical freshwater species and the development of a duration-based water quality guideline; citation_author=AC Hogan, MA Trenfield, AJ Harford, RA Dam; citation_volume=32; citation_issue=9; citation_publication_date=2013; citation_pages=1969-1980; citation_doi=10.1002/etc.2251; citation_id=CR29
citation_journal_title=Emerg Infect Dis; citation_title=Pathogenic Elizabethkingia miricola infection in cultured black-spotted frogs, China, 2016; citation_author=R Hu, J Yuan, Y Meng, Z Wang, Z Gu; citation_volume=23; citation_issue=12; citation_publication_date=2017; citation_pages=2055-2059; citation_doi=10.3201/eid2312.170942; citation_id=CR30
citation_journal_title=Ecotoxicol Environ Saf; citation_title=Chronic effects of environmentally-relevant concentrations of lead in Pelophylax nigromaculata tadpoles: threshold dose and adverse effects; citation_author=MY Huang, RY Duan, X Ji; citation_volume=104; citation_publication_date=2014; citation_pages=310-316; citation_doi=10.1016/j.ecoenv.2014.03.027; citation_id=CR31
citation_journal_title=Chemosphere; citation_title=Toxicity of Pb continuous and pulse exposure on intestinal anatomy, bacterial diversity, and metabolites of Pelophylax nigromaculatus in pre-hibernation; citation_author=M Huang, Y Liu, W Dong, Q Zhao, R Duan, X Cao, Y Wan, J Yin, M Yi; citation_volume=290; citation_publication_date=2021; citation_pages=133304; citation_doi=10.1016/j.chemosphere.2021.133304; citation_id=CR32
Integrated wastewater discharge standard of the People’s Republic of China, 1996. China National Standard: Quality Standards for Integrated wastewater discharge of China GB/T 8978-1996 (Beijing).
citation_journal_title=PLoS ONE; citation_title=Piphillin: improved prediction of metagenomic content by direct inference from human microbiomes; citation_author=S Iwai, T Weinmaier, BL Schmidt, DG Albertson, NJ Poloso, K Dabbagh; citation_volume=11; citation_publication_date=2016; citation_pages=e0166104; citation_doi=10.1371/journal.pone.0166104; citation_id=CR34
citation_journal_title=Front Microbiol; citation_title=Host and aquatic environment shape the amphibian skin microbiome but effects on downstream resistance to the pathogen Batrachochytrium dendrobatidis are variable; citation_author=AJ Jani, CJ Briggs; citation_volume=9; citation_publication_date=2018; citation_pages=487; citation_doi=10.3389/fmicb.2018.00487; citation_id=CR35
citation_journal_title=Proc Natl Acad Sci; citation_title=Stochastic microbiome assembly depends on context; citation_author=EW Jones, JM Carlson, DA Sivak, WB Ludington; citation_volume=119; citation_issue=7; citation_publication_date=2022; citation_pages=e2115877119; citation_doi=10.1073/pnas.2115877119; citation_id=CR36
citation_journal_title=Biomolecules; citation_title=Multidirectional changes in parameters related to sulfur metabolism in frog tissues exposed to heavy metal-related stress; citation_author=M Kaczor-Kamińska, P Sura, M Wróbel; citation_volume=10; citation_issue=4; citation_publication_date=2020; citation_pages=574; citation_doi=10.3390/biom10040574; citation_id=CR37
citation_journal_title=Environ Monit Assess; citation_title=Metal pollution assessment of sediment and water in the Shur River; citation_author=AR Karbassi, SM Monavari, GR Nabi Bidhendi, J Nouri, K Nematpour; citation_volume=147; citation_issue=1–3; citation_publication_date=2008; citation_pages=107-116; citation_doi=10.1007/s10661-007-0102-8; citation_id=CR38
citation_journal_title=Fish Shellfish Immunol; citation_title=Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics; citation_author=DH Kim, B Austin; citation_volume=21; citation_issue=5; citation_publication_date=2006; citation_pages=513-524; citation_doi=10.1016/j.fsi.2006.02.007; citation_id=CR39
citation_journal_title=Ecotoxicol Environ Saf; citation_title=The lead accumulation and hematological findings in juvenile rock fish Sebastes schlegelii exposed to the dietary lead (II) concentrations; citation_author=JH Kim, JC Kang; citation_volume=115; citation_publication_date=2015; citation_pages=33-39; citation_doi=10.1016/j.ecoenv.2015.02.009; citation_id=CR40
citation_journal_title=Int J Syst Evol Microbiol; citation_title=Transfer of Chryseobacterium meningosepticum and Chryseobacterium miricola to Elizabethkingia gen. nov. as Elizabethkingia meningoseptica comb. nov. and Elizabethkingia miricola comb. nov; citation_author=KK Kim, MK Kim, JH Lim, HY Park, ST Lee; citation_volume=55; citation_issue=Pt 3; citation_publication_date=2005; citation_pages=1287-1293; citation_doi=10.1099/ijs.0.63541-0; citation_id=CR41
citation_journal_title=JAMA; citation_title=The microbiome and risk for obesity and diabetes; citation_author=AL Komaroff; citation_volume=317; citation_issue=4; citation_publication_date=2017; citation_pages=355-356; citation_doi=10.1001/jama.2016.20099; citation_id=CR42
citation_journal_title=Front Microbiol; citation_title=Frog skin microbiota vary with host species and environment but not chytrid infection; citation_author=A Kruger; citation_volume=11; citation_publication_date=2020; citation_pages=1330; citation_doi=10.3389/fmicb.2020.01330; citation_id=CR43
citation_journal_title=Mol Ecol; citation_title=The amphibian skin-associated microbiome across species, space and life history stages; citation_author=JG Kueneman, LW Parfrey, DC Woodhams, HM Archer, R Knight, VJ McKenzie; citation_volume=23; citation_issue=6; citation_publication_date=2014; citation_pages=1238-1250; citation_doi=10.1111/mec.12510; citation_id=CR44
citation_journal_title=Biol Conserv; citation_title=Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa; citation_author=BA Lam, JB Walke, VT Vredenburg, RN Harris; citation_volume=143; citation_publication_date=2010; citation_pages=529-531; citation_doi=10.1016/j.biocon.2009.11.01; citation_id=CR45
citation_journal_title=Nat Biotechnol; citation_title=Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences; citation_author=MG Langille, J Zaneveld, JG Caporaso, D McDonald, D Knights, JA Reyes, JC Clemente, DE Burkepile, RL Vega Thurber, R Knight, RG Beiko, C Huttenhower; citation_volume=31; citation_issue=9; citation_publication_date=2013; citation_pages=814-821; citation_doi=10.1038/nbt.2676; citation_id=CR46
citation_journal_title=Transbound Emerg Dis; citation_title=Elizabethkingia miricola infection in Chinese spiny frog (Quasipaa spinosa); citation_author=XP Lei, G Yi, KY Wang, P OuYang, F Chen, XL Huang, C Huang, WM Lai, ZJ Zhong, CL Huo, ZX Yang; citation_volume=66; citation_issue=2; citation_publication_date=2019; citation_pages=1049-1053; citation_doi=10.1111/tbed.13101; citation_id=CR47
citation_journal_title=Chemosphere; citation_title=Zebrafish behavioral phenomics applied for phenotyping aquatic neurotoxicity induced by lead contaminants of environmentally relevant level; citation_author=X Li, H Kong, X Ji, Y Gao, M Jin; citation_volume=224; citation_publication_date=2019; citation_pages=445-454; citation_doi=10.1016/j.chemosphere.2019.02.174; citation_id=CR48
citation_journal_title=J Ethnopharmacol; citation_title=Topical effects of frog “Rana ridibunda” skin secretions on wound healing and reduction of wound microbial load; citation_author=M Mashreghi, M Rezazade Bazaz, N Mahdavi Shahri, A Asoodeh, M Mashreghi, M Behnam Rassouli, S Golmohammadzadeh; citation_volume=145; citation_issue=3; citation_publication_date=2013; citation_pages=793-797; citation_doi=10.1016/j.jep.2012.12.016; citation_id=CR49
citation_journal_title=ISME J; citation_title=Co-habiting amphibian species harbor unique skin bacterial communities in wild populations; citation_author=VJ McKenzie, RM Bowers, N Fierer, R Knight, CL Lauber; citation_volume=6; citation_issue=3; citation_publication_date=2012; citation_pages=588-596; citation_doi=10.1038/ismej.2011.129; citation_id=CR50
citation_journal_title=Ecotoxicol Environ Saf; citation_title=The effect of cadmium exposure on diversity of intestinal microbial community of Rana chensinensis, tadpoles; citation_author=D Mu, J Meng, X Bo, M Wu, H Xiao, H Wang; citation_volume=154; citation_publication_date=2018; citation_pages=6; citation_doi=10.1016/j.ecoenv.2018.02.022; citation_id=CR51
citation_journal_title=J Chem Ecol; citation_title=Synergistic inhibition of the lethal fungal pathogen Batrachochytrium dendrobatidis: the combined effect of symbiotic bacterial metabolites and antimicrobial peptides of the frog Rana muscosa; citation_author=JM Myers, JP Ramsey, AL Blackman, AE Nichols, KP Minbiole, RN Harris; citation_volume=38; citation_issue=8; citation_publication_date=2012; citation_pages=958-965; citation_doi=10.1007/s10886-012-0170-2; citation_id=CR52
citation_journal_title=Ann Glob Health; citation_title=A review of heavy metal contamination of food crops in Nigeria; citation_author=MM Onakpa, AA Njan, OC Kalu; citation_volume=84; citation_issue=3; citation_publication_date=2018; citation_pages=488-494; citation_doi=10.29024/aogh.2314; citation_id=CR53
citation_journal_title=Semin Avian Exot Pet Med; citation_title=An overview of amphibian skin disease; citation_author=AP Pessier, D Acvp; citation_volume=11; citation_publication_date=2002; citation_pages=162-174; citation_doi=10.1053/saep.2002.123980; citation_id=CR54
citation_journal_title=Braz J Biol = Revista brasleira de biologia; citation_title=Isolation and characterization of Flavobacterium columnare (Bernardet et al. 2002) from four tropical fish species in Brazil; citation_author=F Pilarski, AJ Rossini, PS Ceccarelli; citation_volume=68; citation_issue=2; citation_publication_date=2008; citation_pages=409-414; citation_doi=10.1590/s1519-69842008000200025; citation_id=CR55
citation_journal_title=Infect Immun; citation_title=Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus Laevis; citation_author=JP Ramsey, LK Reinert, LK Harper, DC Woodhams, LA Rollins-Smith; citation_volume=78; citation_issue=9; citation_publication_date=2010; citation_pages=3981-3992; citation_doi=10.1128/IAI.00402-10; citation_id=CR56
citation_journal_title=Integr Comp Biol; citation_title=Amphibian immune defenses against chytridiomycosis: impacts of changing environments; citation_author=LA Rollins-Smith, JP Ramsey, JD Pask, LK Reinert, DC Woodhams; citation_volume=51; citation_issue=4; citation_publication_date=2011; citation_pages=552-562; citation_doi=10.1093/icb/icr095; citation_id=CR57
citation_journal_title=Microbiome; citation_title=The skin microbiome of vertebrates; citation_author=AA Ross, A Rodrigues Hoffmann, JD Neufeld; citation_volume=7; citation_issue=1; citation_publication_date=2019; citation_pages=79; citation_doi=10.1186/s40168-019-0694-6; citation_id=CR58
citation_journal_title=Sci Total Environ; citation_title=Bioaccumulation kinetics of copper in Ruditapes philippinarum exposed to increasing, continuous and pulsed exposure: Implications for growth; citation_author=LMBM Santana, J Blasco, DMS Abessa, O Campana; citation_volume=595; citation_publication_date=2017; citation_pages=920-927; citation_doi=10.1016/j.scitotenv.2017.03.020; citation_id=CR59
citation_journal_title=Genome Biol; citation_title=Metagenomic biomarker discovery and explanation; citation_author=N Segata, J Izard, L Waldron, D Gevers, L Miropolsky, WS Garrett, C Huttenhower; citation_volume=12; citation_issue=6; citation_publication_date=2011; citation_pages=R60; citation_doi=10.1186/gb-2011-12-6-r60; citation_id=CR60
citation_journal_title=Aquaculture; citation_title=Characterization and pathogenicity study of Chryseobacterium scophthalmum recovered from gill lesions of diseased golden mahseer, Tor putitora (Hamilton, 1822) in India; citation_author=N Shahi, P Sharma, J Pandey, I Bisht, K Sumanta, null Mallik; citation_volume=485; citation_publication_date=2018; citation_pages=81-92; citation_doi=10.1016/j.aquaculture.2017.11.018; citation_id=CR61
citation_journal_title=Environ Toxicol Pharmacol; citation_title=Acute toxic effects of lead (Pb2+) exposure to rare minnow (Gobiocypris rarus) revealed by histopathological examination and transcriptome analysis; citation_author=L Shi, N Wang, X Hu, D Yin, C Wu, H Liang, W Cao, H Cao; citation_volume=78; citation_publication_date=2020; citation_pages=103385; citation_doi=10.1016/j.etap.2020.103385; citation_id=CR62
citation_journal_title=Ecotoxicol Environ Saf; citation_title=Short-term cadmium exposure induces stress responses in frog (Pelophylax bergeri) skin organ culture; citation_author=F Simoncelli, S Belia, I Rosa, R Paracucchi, R Rossi, G Porta, L Lucentini, A Fagotti; citation_volume=122; citation_publication_date=2015; citation_pages=221-229; citation_doi=10.1016/j.ecoenv.2015.08.001; citation_id=CR63
citation_journal_title=PLoS ONE; citation_title=Skin mucosome activity as an indicator of Batrachochytrium salamandrivorans susceptibility in salamanders; citation_author=HK Smith, F Pasmans, M Dhaenens, D Deforce, D Bonte, K Verheyen, L Lens, A Martel; citation_volume=13; citation_issue=7; citation_publication_date=2018; citation_pages=e0199295; citation_doi=10.1371/journal.pone.0199295; citation_id=CR64
citation_journal_title=Environ Toxicol Chem; citation_title=Effects of chronic cadmium exposure on metamorphosis, skeletal development, and thyroid endocrine disruption in Chinese toad Bufo gargarizans tadpoles; citation_author=N Sun, H Wang, Z Ju, H Zhao; citation_volume=37; citation_issue=1; citation_publication_date=2018; citation_pages=213-223; citation_doi=10.1002/etc.3947; citation_id=CR65
citation_journal_title=Sci Rep; citation_title=Skin bacteria of rainbow trout antagonistic to the fish pathogen Flavobacterium psychrophilum; citation_author=M Takeuchi, E Fujiwara-Nagata, T Katayama, H Suetake; citation_volume=11; citation_issue=1; citation_publication_date=2021; citation_pages=7518; citation_doi=10.1038/s41598-021-87167-1; citation_id=CR66
Tchounwou PB, Yedjou CG, Patlolla AK, Suthon D (2012) Heavy metals toxicity and the environment. Mol Clin Environ Toxicol 101:133–164.
https://doi.org/10.1007/978-3-7643-8340-4_6
citation_journal_title=Comp Biochem Physiol; citation_title=Cutaneous granular glands and amphibian venoms; citation_author=RC Toledo, C Jared; citation_volume=111; citation_publication_date=1995; citation_pages=1-29; citation_doi=10.1016/0300-9629(95)98515-I; citation_id=CR68
citation_journal_title=Front Immunol; citation_title=Frog skin innate immune defences: sensing and surviving pathogens; citation_author=J Varga, MP Bui-Marinos, BA Katzenback; citation_volume=9; citation_publication_date=2019; citation_pages=3128; citation_doi=10.3389/fimmu.2018.03128; citation_id=CR69
citation_journal_title=FEMS Microbiol Lett; citation_title=Individual variation of natural D. melanogaster-associated bacterial communities; citation_author=Y Wang, F Staubach; citation_volume=365; citation_issue=6; citation_publication_date=2018; citation_pages=fny017; citation_doi=10.1093/femsle/fny017; citation_id=CR70
citation_journal_title=Sci Total Environ; citation_title=Multivariate statistical evaluation of dissolved trace elements and a water quality assessment in the middle reaches of Huaihe River, Anhui, China; citation_author=J Wang, G Liu, H Liu, PKS Lam; citation_volume=583; citation_publication_date=2017; citation_pages=421-431; citation_doi=10.1016/j.scitotenv.2017.01.088; citation_id=CR71
citation_journal_title=Ecol Ind; citation_title=The effect of fluorine exposure on morphological indicators and intestinal microbial community in Bufo gargarizans tadpoles; citation_author=X Wang, X Bo, Q Yao, M Wu, H Wang; citation_volume=98; citation_publication_date=2019; citation_pages=763-771; citation_doi=10.1016/j.ecolind.2018.11.070; citation_id=CR72
citation_journal_title=Behav Brain Sci; citation_title=Inter-individual variation shapes the human microbiome; citation_author=EF Wissel, LK Smith; citation_volume=42; citation_publication_date=2019; citation_pages=E79; citation_doi=10.1017/S0140525X1800287X; citation_id=CR73
citation_journal_title=PLoS ONE; citation_title=Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness; citation_author=DC Woodhams, H Brandt, S Baumgartner, J Kielgast, E Küpfer, U Tobler, LR Davis, BR Schmidt, C Bel, S Hodel, R Knight, V McKenzie; citation_volume=9; citation_issue=4; citation_publication_date=2014; citation_pages=e96375; citation_doi=10.1371/journal.pone.0096375; citation_id=CR74
citation_journal_title=BMC Microbiol; citation_title=Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis; citation_author=L Wu, C Wen, Y Qin, H Yin, Q Tu, JD Nostrand, T Yuan, M Yuan, Y Deng, J Zhou; citation_volume=15; citation_publication_date=2015; citation_pages=125; citation_doi=10.1186/s12866-015-0450-4; citation_id=CR75
citation_journal_title=Toxicol Sci; citation_title=Perinatal lead exposure alters gut microbiota composition and results in sex-specific bodyweight increases in adult mice; citation_author=J Wu, XW Wen, C Faulk, K Boehnke, H Zhang, DC Dolinoy, C Xi; citation_volume=151; citation_publication_date=2016; citation_pages=324-333; citation_doi=10.1093/toxsci/kfw046; citation_id=CR76
citation_journal_title=Sci Total Environ; citation_title=Chronic exposure to low concentrations of lead induces metabolic disorder and dysbiosis of the gut microbiota in mice; citation_author=J Xia, C Jin, Z Pan, L Sun, Z Fu, Y Jin; citation_volume=631–632; citation_publication_date=2018; citation_pages=439-448; citation_doi=10.1016/j.scitotenv.2018.03.053; citation_id=CR77
citation_journal_title=Ecotoxicol Environ Saf; citation_title=The effects of chronic cadmium exposure on the gut of Bufo gargarizans larvae at metamorphic climax: histopathological impairments, microbiota changes and intestinal remodeling disruption; citation_author=J Ya, X Li, L Wang, H Kou, H Wang, H Zhao; citation_volume=195; citation_publication_date=2020; citation_pages=110523; citation_doi=10.1016/j.ecoenv.2020.110523; citation_id=CR78
citation_journal_title=Chemosphere; citation_title=Probing the effects of hexavalent chromium exposure on histology and fatty acid metabolism in liver of Bufo gargarizans tadpoles; citation_author=Y Yang, W Wang, X Liu, X Song, L Chai; citation_volume=243; citation_publication_date=2020; citation_pages=125437; citation_doi=10.1016/j.chemosphere.2019.125437; citation_id=CR79
citation_journal_title=Chemosphere; citation_title=Effects of hexavalent chromium on intestinal histology and microbiota in Bufo gargarizans tadpoles; citation_author=Q Yao, H Yang, X Wang, H Wang; citation_volume=216; citation_publication_date=2019; citation_pages=313-323; citation_doi=10.1016/j.chemosphere.2018.10.147; citation_id=CR80
citation_journal_title=Circulation; citation_title=Bacteroides vulgatus and Bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis; citation_author=N Yoshida, T Emoto, T Yamashita, H Watanabe, T Hayashi, T Tabata, N Hoshi, N Hatano, G Ozawa, N Sasaki, T Mizoguchi, HZ Amin, Y Hirota, W Ogawa, T Yamada, KI Hirata; citation_volume=138; citation_issue=22; citation_publication_date=2018; citation_pages=2486-2498; citation_doi=10.1161/circlulationaha.118.033714; citation_id=CR81
citation_journal_title=Sci Bull; citation_title=Effects of subchronic oral toxic metal exposure on the intestinal microbiota of mice; citation_author=Q Zhai, T Li, L Yu, Y Xiao, S Feng, J Wu, J Zhao, H Zhang, W Chen; citation_volume=62; citation_publication_date=2017; citation_pages=831-840; citation_doi=10.1016/j.scib.2017.01.031; citation_id=CR82
citation_journal_title=Ecotoxicol Environ Saf; citation_title=The response of larvae Brachymystax lenok during continuous and single pulses exposure to copper, zinc, lead and cadmium; citation_author=F Zhang, J Xu; citation_volume=165; citation_publication_date=2018; citation_pages=153-159; citation_doi=10.1016/j.ecoenv.2018.08.091; citation_id=CR83
citation_journal_title=Environ Sci Pollut Res; citation_title=Reconstruction of historical lead contamination and sources in Lake Hailing, Eastern China: a Pb isotope study; citation_author=R Zhang, M Guan, Y Shu, L Shen, X Chen, F Zhang, T Li, T Jiang; citation_volume=23; citation_issue=9; citation_publication_date=2016; citation_pages=9183-9191; citation_doi=10.1007/s11356-016-6166-7; citation_id=CR84
citation_journal_title=Environ Sci Pollut Res; citation_title=Effects of atrazine short-term exposure on jumping ability and intestinal microbiota diversity in male Pelophylax nigromaculatus adults; citation_author=Q Zhao, M Huang, Y Liu, Y Wan, R Duan, L Wu; citation_volume=28; citation_issue=27; citation_publication_date=2021; citation_pages=36122-36132; citation_doi=10.1007/s11356-021-13234-9; citation_id=CR85
citation_journal_title=Chemosphere; citation_title=Intestinal response characteristic and potential microbial dysbiosis in digestive tract of Bufo gargarizans after exposure to cadmium and lead, alone or combined; citation_author=R Zheng, P Wang, B Cao, M Wu, X Li, H Wang, L Chai; citation_volume=271; citation_publication_date=2021; citation_pages=129511; citation_doi=10.1016/j.chemosphere.2020.129511; citation_id=CR86