Abstract
The selective pressure of the living surroundings is a key factor in the development of resistance profiles in pathogenic bacteria such as Aeromonas spp. In this study, Aeromonas species were isolated from the Ba River, and their composition, resistance profiles to antibiotics, and heavy metals (HMs) were investigated. The discovery revealed that selective pressure altered the diversity of Aeromonas spp., with Aeromonas veronii being more adaptable to contaminated waters. Long-term exposure to antibiotics or HMs exerts persistent selective pressure on Aeromonas species, leading to the increase in multiple antibiotic resistance (MAR) index and multidrug-resistant (MDR) strains. Furthermore, HMs could drive the co-selection of antibiotic resistance via co-resistance or cross-resistance. blaTEM, blaSHV, blaCTX-M, sul1, czcA, mexA, and mexF were detected at high frequencies in Aeromonas species. Among these resistance phenotypes conferred genes, blaTEM may be intrinsic in the genome of Aeromonas spp., while mexA and mexF may have been acquired from surrounding environments owing to selective pressure. Resistance genes evolved as a consequence of selective pressure and have been shown to be positively correlated with their prevalence. Our study suggests that the selective pressure of living surroundings significantly contributes to the composition and resistance profiles of Aeromonas spp. in the riverine ecosystem.
Similar content being viewed by others
Data availability
Not applicable.
References
Altwegg M, Geiss HK (1989) Aeromonas as a human pathogen. Crit Rev Microbiol 16(4):253–286. https://doi.org/10.3109/10408418909105478
Araujo RM, Arribas RM, Pares R (1991) Distribution of Aeromonas species in waters with different levels of pollution. J Appl Bacteriol 71(2):182–186. https://doi.org/10.1111/j.1365-2672.1991.tb02976.x
Balsalobre LC, Dropa M, de Oliveira DE, Lincopan N, Mamizuka EM, Matté GR, Matté MH (2010) Presence of bla TEM-116 gene in environmental isolates of Aeromonas hydrophila and Aeromonas jandaei from Brazil. Braz J Microbiol 41(3):718–719. https://doi.org/10.1590/s1517-83822010000300023
Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45(4):493–496
Bostanghadiri N, Ghalavand Z, Fallah F, Yadegar A, Ardebili A, Tarashi S, Pournajaf A, Mardaneh J, Shams S, Hashemi A (2019) Characterization of phenotypic and genotypic diversity of Stenotrophomonas maltophilia strains isolated from selected hospitals in Iran. Front Microbiol 10:1191. https://doi.org/10.3389/fmicb.2019.01191
Bradford PA 2001 Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev, 14(4), 933–51, table of contents. https://doi.org/10.1128/cmr.14.4.933-951.2001
Chen H, Bai X, Jing L, Chen R, Teng Y (2019) Characterization of antibiotic resistance genes in the sediments of an urban river revealed by comparative metagenomics analysis. Sci Total Environ 653:1513–1521. https://doi.org/10.1016/j.scitotenv.2018.11.052
Choudhury D, Ghose A, Dhar Chanda D, Das Talukdar A, Dutta Choudhury M, Paul D, Maurya AP, Chakravarty A, Bhattacharjee A (2016) Premature termination of MexR leads to overexpression of MexAB-OprM efflux pump in Pseudomonas aeruginosa in a tertiary referral hospital in India. PLoS One 11(2):e0149156. https://doi.org/10.1371/journal.pone.0149156
Danner MC, Robertson A, Behrends V, Reiss J (2019) Antibiotic pollution in surface fresh waters: occurrence and effects. Sci Total Environ 664:793–804. https://doi.org/10.1016/j.scitotenv.2019.01.406
Deng YT, Wu YL, Tan AP, Huang YP, Jiang L, Xue HJ, Wang WL, Luo L, Zhao F (2014) Analysis of antimicrobial resistance genes in Aeromonas spp. isolated from cultured freshwater animals in China. Microb Drug Resist 20(4):350–6. https://doi.org/10.1089/mdr.2013.0068
Glibota N, Grande Burgos MJ, Gálvez A, Ortega E (2019) Copper tolerance and antibiotic resistance in soil bacteria from olive tree agricultural fields routinely treated with copper compounds. J Sci Food Agric 99(10):4677–4685. https://doi.org/10.1002/jsfa.9708
Guan Y, Jia J, Wu L, Xue X, Zhang G, Wang Z (2018) Analysis of bacterial community characteristics, abundance of antibiotics and antibiotic resistance genes along a pollution gradient of Ba River in Xi’an, China. Front Microbiol 9:3191. https://doi.org/10.3389/fmicb.2018.03191
Huang YH, Liu Y, Du PP, Zeng LJ, Mo CH, Li YW, Lü H, Cai QY (2019) Occurrence and distribution of antibiotics and antibiotic resistant genes in water and sediments of urban rivers with black-odor water in Guangzhou, South China. Sci Total Environ 670:170–180. https://doi.org/10.1016/j.scitotenv.2019.03.168
Imran M, Das KR, Naik MM (2019) Co-selection of multi-antibiotic resistance in bacterial pathogens in metal and microplastic contaminated environments: an emerging health threat. Chemosphere 215:846–857. https://doi.org/10.1016/j.chemosphere.2018.10.114
Jacob ME, Fox JT, Nagaraja TG, Drouillard JS, Amachawadi RG, Narayanan SK (2010) Effects of feeding elevated concentrations of copper and zinc on the antimicrobial susceptibilities of fecal bacteria in feedlot cattle. Foodborne Pathog Dis 7(6):643–648. https://doi.org/10.1089/fpd.2009.0401
Janda JM, Abbott SL (2010) The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23(1):35–73. https://doi.org/10.1128/cmr.00039-09
Jia J, Cheng M, Xue X, Guan Y, Wang Z (2020) Characterization of tetracycline effects on microbial community, antibiotic resistance genes and antibiotic resistance of Aeromonas spp. in gut of goldfish Carassius auratus Linnaeus. Ecotoxicol Environ Saf 191:110182. https://doi.org/10.1016/j.ecoenv.2020.110182
Jia J, Guan Y, Cheng M, Chen H, He J, Wang S, Wang Z (2018) Occurrence and distribution of antibiotics and antibiotic resistance genes in Ba River, China. Sci Total Environ 642:1136–1144. https://doi.org/10.1016/j.scitotenv.2018.06.149
Karmakar R, Bindiya S, Hariprasad P (2019) Convergent evolution in bacteria from multiple origins under antibiotic and heavy metal stress, and endophytic conditions of host plant. Sci Total Environ 650(Pt 1):858–867. https://doi.org/10.1016/j.scitotenv.2018.09.078
Köchl S, Niederstätter H, Parson W (2005) DNA extraction and quantitation of forensic samples using the phenol-chloroform method and real-time PCR. Methods Mol Biol 297:13–30. https://doi.org/10.1385/1-59259-867-6:013
Krumperman PH (1983) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 46(1):165–170. https://doi.org/10.1128/aem.46.1.165-170.1983
Kumar V, Parihar RD, Sharma A, Bakshi P, Singh Sidhu GP, Bali AS, Karaouzas I, Bhardwaj R, Thukral AK, Gyasi-Agyei Y, Rodrigo-Comino J (2019) Global evaluation of heavy metal content in surface water bodies: a meta-analysis using heavy metal pollution indices and multivariate statistical analyses. Chemosphere 236:124364. https://doi.org/10.1016/j.chemosphere.2019.124364
Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, Krishnan P, Kumar AV, Maharjan S, Mushtaq S, Noorie T, Paterson DL, Pearson A, Perry C, Pike R, Rao B, Ray U, Sarma JB, Sharma M, Sheridan E, Thirunarayan MA, Turton J, Upadhyay S, Warner M, Welfare W, Livermore DM, Woodford N (2010) Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 10(9):597–602. https://doi.org/10.1016/s1473-3099(10)70143-2
Lei K, Zhu Y, Chen W, Pan HY, Cao YX, Zhang X, Guo BB, Sweetman A, Lin CY, Ouyang W, He MC, Liu XT (2019) Spatial and seasonal variations of antibiotics in river waters in the Haihe River Catchment in China and ecotoxicological risk assessment. Environ Int 130:104919. https://doi.org/10.1016/j.envint.2019.104919
Levin-Reisman I, Ronin I, Gefen O, Braniss I, Shoresh N, Balaban NQ (2017) Antibiotic tolerance facilitates the evolution of resistance. Science 355(6327):826–830. https://doi.org/10.1126/science.aaj2191
Li H, Li Y, Ming-Kuo L, Liu Z, Miao C (2015) Spatiotemporal analysis of heavy metal water pollution in transitional China. Sustainability 7(7):91–94. https://doi.org/10.1016/j.jhydrol.2018.02.081
Maruzani R, Pathak A, Ward M, Serafim V, Marvasi M (2020) Antibiotic selective pressure in microcosms: pollution influences the persistence of multidrug resistant Shigella flexneri 2a YSH6000 strain in polluted river water samples. Environ Technol Innov 19:100821. https://doi.org/10.1016/j.eti.2020.100821
Mather LE, Austin KL (1983) The Statistical Package for the Social Sciences (SPSS) as an adjunct to pharmacokinetic analysis. Biopharm Drug Dispos 4(2):157–172. https://doi.org/10.1002/bdd.2510040208
Mirzaei R, Mesdaghinia A, Hoseini SS, Yunesian M (2019) Antibiotics in urban wastewater and rivers of Tehran, Iran: consumption, mass load, occurrence, and ecological risk. Chemosphere 221:55–66. https://doi.org/10.1016/j.chemosphere.2018.12.187
Patil HJ, Benet-Perelberg A, Naor A, Smirnov M, Ofek T, Nasser A, Minz D, Cytryn E (2016) Evidence of increased antibiotic resistance in phylogenetically-diverse Aeromonas isolates from semi-intensive fish ponds treated with antibiotics. Front Microbiol 7:1875. https://doi.org/10.3389/fmicb.2016.01875
Philip D (2003) VEGAN a package of R functions for community ecology. J Veg Sci 14(6):927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
Piotrowska M, Popowska M (2015) Insight into the mobilome of Aeromonas strains. Front Microbiol 6:494. https://doi.org/10.3389/fmicb.2015.00494
Puja H, Bolard A, Noguès A, Plésiat P, Jeannot K 2020 The efflux pump MexXY/OprM contributes to the tolerance and acquired resistance of Pseudomonas aeruginosa to colistin. Antimicrob Agents Chemother, 64(4). https://doi.org/10.1128/aac.02033-19
Qiu W, Sun J, Fang M, Luo S, Tian Y, Dong P, Xu B, Zheng C (2019) Occurrence of antibiotics in the main rivers of Shenzhen, China: association with antibiotic resistance genes and microbial community. Sci Total Environ 653:334–341. https://doi.org/10.1016/j.scitotenv.2018.10.398
Radu S, Ahmad N, Ling FH, Reezal A (2003) Prevalence and resistance to antibiotics for Aeromonas species from retail fish in Malaysia. Int J Food Microbiol 81(3):261–266. https://doi.org/10.1016/s0168-1605(02)00228-3
Richardot C, Juarez P, Jeannot K, Patry I, Plésiat P, Llanes C (2016) Amino acid substitutions account for most MexS alterations in clinical nfxC mutants of Pseudomonas aeruginosa. Antimicrob Agents Chemother 60(4):2302–2310. https://doi.org/10.1128/aac.02622-15
Scarano C, Piras F, Virdis S, Ziino G, Nuvoloni R, Dalmasso A, De Santis EPL, Spanu C (2018) Antibiotic resistance of Aeromonas ssp. strains isolated from Sparus aurata reared in Italian mariculture farms. Int J Food Microbiol 284:91–97. https://doi.org/10.1016/j.ijfoodmicro.2018.07.033
Sekomo B, Christian N, Kikongo M-M, Bahati J, Manegabe J (2017) Antibiotic resistance and tolerance to heavy metals demonstrated by environmental pathogenic bacteria isolated from the Kahwa River, Bukavu Town, Democratic Republic of the Congo. Int J Environ Stud 74(2):290–302
Sheeba VA, Anas A, Jasmin C, Vincent M, Parameswaran PS (2020) Response of particle-associated bacteria to long-term heavy metal contamination in a tropical estuary. World J Microbiol Biotechnol 36(5):65. https://doi.org/10.1007/s11274-020-02842-1
Sundar K, Vidya R, Mukherjee A, Chandrasekaran N (2010) High chromium tolerant bacterial strains from Palar River Basin: impact of tannery pollution. Res J Environ Earth Sci 2(2):112–117
Taylor NG, Verner-Jeffreys DW, Baker-Austin C (2011) Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance? Trends Ecol Evol 26(6):278–284. https://doi.org/10.1016/j.tree.2011.03.004
Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, Laxminarayan R (2014) Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14(8):742–750. https://doi.org/10.1016/s1473-3099(14)70780-7
Wang G, Zhou S, Han X, Zhang L, Ding S, Li Y, Zhang D, Zarin K (2020) Occurrence, distribution, and source track of antibiotics and antibiotic resistance genes in the main rivers of Chongqing city Southwest China. J Hazard Mater 389:122110. https://doi.org/10.1016/j.jhazmat.2020.122110
Wang Y, Lu J, Mao L, Li J, Yuan Z, Bond PL, Guo J (2019) Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacterial genera. Isme j 13(2):509–522. https://doi.org/10.1038/s41396-018-0275-x
Wiegand I, Hilpert K, Hancock RE (2008) Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 3(2):163–175. https://doi.org/10.1038/nprot.2007.521
Wu D, Huang Z, Yang K, Graham D, Xie B (2015) Relationships between antibiotics and antibiotic resistance gene levels in municipal solid waste leachates in Shanghai, China. Environ Sci Technol 49(7):4122–4128. https://doi.org/10.1021/es506081z
Xu K, Wang J, Gong H, Li Y, Zhou L, Yan M (2019) Occurrence of antibiotics and their associations with antibiotic resistance genes and bacterial communities in Guangdong coastal areas. Ecotoxicol Environ Saf 186:109796. https://doi.org/10.1016/j.ecoenv.2019.109796
Yáñez MA, Catalán V, Apráiz D, Figueras MJ, Martínez-Murcia AJ (2003) Phylogenetic analysis of members of the genus Aeromonas based on gyrB gene sequences. Int J Syst Evol Microbiol 53(Pt 3):875–883. https://doi.org/10.1099/ijs.0.02443-0
Yi X, Wang M, Zhou Z (2019) The potential impact of naturally produced antibiotics, environmental factors, and anthropogenic pressure on the occurrence of erm genes in urban soils. Environ Pollut 245:282–289. https://doi.org/10.1016/j.envpol.2018.11.009
Funding
This work was supported by grant from the National Natural Science Foundation of China (31870487).
Author information
Authors and Affiliations
Contributions
JJ: conceptualization, investigation, project administration, writing—original draft; ZZ: investigation, methodology; XX: investigation, project administration; XX: investigation, formal analysis; XL: resources, formal analysis; ZW: supervision, funding acquisition, validation, writing—review and editing.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Diane Purchase
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jia, J., Zhu, Z., Xue, X. et al. Selective pressure governs the composition, antibiotic, and heavy metal resistance profiles of Aeromonas spp. isolated from Ba River in Northwest China. Environ Sci Pollut Res 29, 75841–75850 (2022). https://doi.org/10.1007/s11356-022-20678-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-20678-0