The meiofauna as neglected carriers of antibiotic resistant and pathogenic bacteria in freshwater ecosystems

Submitted: 8 August 2021
Accepted: 22 November 2021
Published: 29 November 2021
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The World Health Organization considers antibiotic resistance as one of the main threats to human and other animals' health. Despite the measures used to limit the spread of antibiotic resistance, the efforts made are not enough to tackle this problem. Thus, it has become important to understand how bacteria acquire and transmit antibiotic resistant genes (ARGs), in particular in the environment, given the close connection between the latter and human and animal health, as defined by the One-Health concept. Aquatic ecosystems are often strongly impacted by anthropogenic activities, making them a source for ARGs and antibiotic resistant bacteria (ARB). Although freshwater meiofauna have been the object of active research, few studies have focused on the relationship between the spread of antibiotic resistance and these organisms. In this review, we investigated freshwater meiofauna as carriers of resistances since they play a central role in the aquatic environments and can harbor human and animal potential pathogens. We assessed if these animals could contribute to the spread of ARGs and of potentially pathogenic bacteria. Only four taxa (Rotifera, Chironomidae, Cladocera, Copepoda) were found to be the subject of studies focused on antibiotic resistance. The studies we analyzed, although with some limitations, demonstrated that ARGs and ARB can be found in these animals, and several of them showed the presence of potentially pathogenic bacteria for humans and animals within their microbiome. Thus, meiofauna can be considered a source and a reservoir, even if neglected, of ARGs and ARB for the freshwater environments. However, further studies are needed to evaluate the impact of the meiofauna on the spread and persistence of antibiotic resistance in these ecosystems.

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Adámek Z, Maršálek B, 2013. Bioturbation of sediments by benthic macroinvertebrates and fish and its implication for pond ecosystems: a review. Aquacult. Int. 21:1–17. DOI: https://doi.org/10.1007/s10499-012-9527-3
Akbar S, Gu L, Sun Y, Zhou Q, Zhang L, Lyu K, Huang Y, Yang Z, 2020. Changes in the life history traits of Daphnia magna are associated with the gut microbiota composition shaped by diet and antibiotics. Sci. Total Environ. 705:135827. DOI: https://doi.org/10.1016/j.scitotenv.2019.135827
Allgaier M, Grossart H-P, 2006. Seasonal dynamics and phylogenetic diversity of free-living and particle-associated bacterial communities in four lakes in northeastern Germany. Aquat. Microb. Ecol. 45:115–128. DOI: https://doi.org/10.3354/ame045115
Alonso C, Pernthaler J, 2005. Incorporation of glucose under anoxic conditions by bacterioplankton from coastal North Sea surface waters. Appl. Environ. Microbiol. 71:1709–1716. DOI: https://doi.org/10.1128/AEM.71.4.1709-1716.2005
Alperi A, Figueras MJ, 2010. Human isolates of Aeromonas possess Shiga toxin genes (stx1 and stx2) highly similar to the most virulent gene variants of Escherichia coli. Clin. Microbiol. Infect. 16:1563–1567. DOI: https://doi.org/10.1111/j.1469-0691.2010.03203.x
Alves AS, Adão H, Ferrero TJ, Marques JC, Costa MJ, Patrício J, 2013. Benthic meiofauna as indicator of ecological changes in estuarine ecosystems: The use of nematodes in ecological quality assessment. Ecol. Indic. 24:462-475. DOI: https://doi.org/10.1016/j.ecolind.2012.07.013
Bass D, Stentiford GD, Wang H-C, Koskella B, Tyler CR, 2019. The pathobiome in animal and plant diseases. Trends Ecol. Evol. 34:996-1008. DOI: https://doi.org/10.1016/j.tree.2019.07.012
Basu A, Hazra N, Ghosh K, 2010. Bioindicator potentiality of the chironomine larvae (Diptera: Chironomidae) for determination of antibiotic resistant microbial load of the aquatic ecosystem. Proc. Zool. Soc. 63:79-86. DOI: https://doi.org/10.1007/s12595-010-0011-7
Beaz-Hidalgo R, Shakèd T, Laviad S, Halpern M, Figueras MJ, 2012. Chironomid egg masses harbour the clinical species Aeromonas taiwanensis and Aeromonas sanarellii. FEMS Microbiol. Lett. 337:48–54. DOI: https://doi.org/10.1111/1574-6968.12003
Bergan T, 1981. Human- and animal-pathogenic members of the genus Pseudomonas, p. 666-700. In: M.P. Starr, H. Stolp, H.G. Trüper, A. Balows and H.G. Schlegel (eds.), The Prokaryotes. Cham, Springer. DOI: https://doi.org/10.1007/978-3-662-13187-9_59
Besser TE, Goldoft M, Pritchett LC, Khakhria R, Hancock DD, Rice DH, Gay JM, Johnson W, Gay CC, 2000. Multiresistant Salmonella Typhimurium DT104 infections of humans and domestic animals in the Pacific Northwest of the United States. Epidemiol. Infect. 124:193–200. DOI: https://doi.org/10.1017/S0950268899003283
Bonaglia S, Nascimento FJA, Bartoli M, Klawonn I, Brüchert V, 2014. Meiofauna increases bacterial denitrification in marine sediments. Nat. Commun. 5:5133. DOI: https://doi.org/10.1038/ncomms6133
Burnham JP, 2021. Climate change and antibiotic resistance: a deadly combination. Ther. Adv. Infect. Dis. 8:1-7. DOI: https://doi.org/10.1177/2049936121991374
Callens M, De Meester L, Muylaert K, Mukherjee S, Decaestecker E, 2020. The bacterioplankton community composition and a host genotype dependent occurrence of taxa shape the Daphnia magna gut bacterial community. FEMS Microbiol. Ecol. 96:fiaa128. DOI: https://doi.org/10.1093/femsec/fiaa128
Callens M, Watanabe H, Kato Y, Miura J, Decaestecker E, 2018. Microbiota inoculum composition affects holobiont assembly and host growth in Daphnia. Microbiome 6:56. DOI: https://doi.org/10.1186/s40168-018-0444-1
Chaix G, Roger F, Berthe T, Lamy B, Jumas-Bilak E, Lafite R, Forget-Leray J, Petit F, 2017. Distinct Aeromonas populations in water column and associated with copepods from estuarine environment (Seine, France). Front. Microbiol. 8:1259. DOI: https://doi.org/10.3389/fmicb.2017.01259
Chao H, Kong L, Zhang H, Sun M, Ye M, Huang D, Zhang Z, Sun D, Zhang S, Yuan Y, Liu M, Hu F, et al., 2019. Metaphire guillelmi gut as hospitable micro-environment for the potential transmission of antibiotic resistance genes. Sci. Total Environ. 669:353–361. DOI: https://doi.org/10.1016/j.scitotenv.2019.03.017
Cooper RO, Cressler CE, 2020. Characterization of key bacterial species in the Daphnia magna microbiota using shotgun metagenomics. Sci. Rep. 10:652. DOI: https://doi.org/10.1038/s41598-019-57367-x
Cooper RO, Vavra JM, Cressler CE, 2021. Targeted manipulation of abundant and rare taxa in the Daphnia magna microbiota with antibiotics impacts host fitness differentially. Msystems 6:e00916-20. DOI: https://doi.org/10.1128/mSystems.00916-20
Dallaire-Dufresne S, Tanaka KH, Trudel MV, Lafaille A, Charette SJ, 2014. Virulence, genomic features, and plasticity of Aeromonas salmonicida subsp. salmonicida, the causative agent of fish furunculosis. Vet. Microbiol. 169:1–7. DOI: https://doi.org/10.1016/j.vetmic.2013.06.025
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, et al., 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559-563. DOI: https://doi.org/10.1038/nature12820
de Kraker MEA, Stewardson AJ, Harbarth S, 2016. Will 10 million people die a year due to antimicrobial resistance by 2050? PLoS Med. 13:e1002184. DOI: https://doi.org/10.1371/journal.pmed.1002184
de Nies L, Lopes S, Busi SB, Galata V, Heintz-Buschart A, Laczny CC, May P, Wilmes P, 2021. PathoFact: a pipeline for the prediction of virulence factors and antimicrobial resistance genes in metagenomic data. Microbiome 9:49. DOI: https://doi.org/10.1186/s40168-020-00993-9
Di Cesare A, Eckert EM, Cottin C, Bouchez A, Callieri C, Cortesini M, Lami A, Corno G, 2020. The vertical distribution of tetA and intI1 in a deep lake is rather due to sedimentation than to resuspension. FEMS Microbiol. Ecol. 96:fiaa002. DOI: https://doi.org/10.1093/femsec/fiaa002
Di Cesare A, Eckert EM, Teruggi A, Fontaneto D, Bertoni R, Callieri C, Corno G, 2015. Constitutive presence of antibiotic resistance genes within the bacterial community of a large subalpine lake. Mol. Ecol. 24:3888-3900. DOI: https://doi.org/10.1111/mec.13293
Ding C, Ma J, Jiang W, Zhao H, Shi M, Cui G, Yan T, Wang Q, Li J, Qiu Z, 2021. Chironomidae larvae: A neglected enricher of antibiotic resistance genes in the food chain of freshwater environments. Environ. Pollut. 285:117486. DOI: https://doi.org/10.1016/j.envpol.2021.117486
Dumont H, Negrea S, 2002. Introduction to the class Branchiopoda. In: Guides to the Identification of the Microinvertebrates of the Continental Waters of the World. Leiden, Backhuys Publ.
Ebert D, 2005. Ecology, Epidemiology, and Evolution of Parasitism in Daphnia. National Center for Biotechnology
Eckert EM, Amalfitano S, Di Cesare A, Manzari C, Corno G, Fontaneto D, 2020. Different substrates within a lake harbour connected but specialised microbial communities. Hydrobiologia 847:1689–1704. DOI: https://doi.org/10.1007/s10750-019-04068-1
Eckert EM, Anicic N, Fontaneto D, 2021. Freshwater zooplankton microbiome composition is highly flexible and strongly influenced by the environment. Mol. Ecol. 30:1545–1558. DOI: https://doi.org/10.1111/mec.15815
Eckert EM, Di Cesare A, Stenzel B, Fontaneto D, Corno G, 2016. Daphnia as a refuge for an antibiotic resistance gene in an experimental freshwater community. Sci. Total Environ. 571:77–81. DOI: https://doi.org/10.1016/j.scitotenv.2016.07.141
Eckert EM, Pernthaler J, 2014. Bacterial epibionts of Daphnia: a potential route for the transfer of dissolved organic carbon in freshwater food webs. ISME J. 8:1808–1819. DOI: https://doi.org/10.1038/ismej.2014.39
Fenchel TM, 1978. The ecology of micro-and meiobenthos. Annu. Rev. Ecol. Syst. 9:99–121. DOI: https://doi.org/10.1146/annurev.es.09.110178.000531
Finley RL, Collignon P, Larsson DGJ, McEwen SA, Li X-Z, Gaze WH, Reid-Smith R, Timinouni M, Graham DW, Topp E, 2013. The scourge of antibiotic resistance: The important role of the environment. Clin. Infect. Dis. 57:704-710. DOI: https://doi.org/10.1093/cid/cit355
Fonseca G, Fontaneto D, Di Domenico M, 2018. Addressing biodiversity shortfalls in meiofauna. J. Exp. Mari. Biol. Ecol. 502:26-38. DOI: https://doi.org/10.1016/j.jembe.2017.05.007
Fontaneto D, 2019. Long-distance passive dispersal in microscopic aquatic animals. Mov. Ecol. 7:10. DOI: https://doi.org/10.1186/s40462-019-0155-7
Fontaneto D, Flot J-F, Tang CQ, 2015. Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar. Biodiv. 45:433-451. DOI: https://doi.org/10.1007/s12526-015-0319-7
Foster JA, McVey Neufeld K-A, 2013. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 36:305-312. DOI: https://doi.org/10.1016/j.tins.2013.01.005
Frankel-Bricker J, Song MJ, Benner MJ, Schaack S, 2020. Variation in the microbiota associated with Daphnia magna across genotypes, populations, and temperature. Microb. Ecol. 79:731–742. DOI: https://doi.org/10.1007/s00248-019-01412-9
Freese HM, Schink B, 2011. Composition and stability of the microbial community inside the digestive tract of the aquatic crustacean Daphnia magna. Microb. Ecol. 4:882–894. DOI: https://doi.org/10.1007/s00248-011-9886-8
Fu J, Yang D, Jin M, Liu W, Zhao X, Li C, Zhao T, Wang J, Gao Z, Shen Z, Qiu Z, Li J-W, 2017. Aquatic animals promote antibiotic resistance gene dissemination in water via conjugation: Role of different regions within the zebra fish intestinal tract, and impact on fish intestinal microbiota. Mol. Ecol. 26:5318–5333. DOI: https://doi.org/10.1111/mec.14255
Garner E, Benitez R, Wagoner E von, Sawyer R, Schaberg E, Hession WC, Krometis L-AH, Badgley BD, Pruden A, 2017. Stormwater loadings of antibiotic resistance genes in an urban stream. Water Res. 123:144–152. DOI: https://doi.org/10.1016/j.watres.2017.06.046
Giere O, 2009. Meiobenthology: The microscopic motile fauna of aquatic sediments. Cham, Springer: 548 pp.
Grossart H-P, Dziallas C, Leunert F, Tang KW, 2010. Bacteria dispersal by hitchhiking on zooplankton. P. Natl. Acad. Sci. USA 107:11959–11964. DOI: https://doi.org/10.1073/pnas.1000668107
Grossart H-P, Dziallas C, Tang KW, 2009. Bacterial diversity associated with freshwater zooplankton. Environ. Microbiol. Rep. 1:50–55. DOI: https://doi.org/10.1111/j.1758-2229.2008.00003.x
Guardabassi L, Butaye P, Dockrell DH, Fitzgerald JR, Kuijper EJ, ESCMID Study Group for Veterinary Microbiology (ESGVM), 2020. One Health: a multifaceted concept combining diverse approaches to prevent and control antimicrobial resistance. Clin. Microbiol. Infect. 26:1604-1605. DOI: https://doi.org/10.1016/j.cmi.2020.07.012
Halpern M, Senderovich Y, 2015. Chironomid microbiome. Microb. Ecol. 70:1-8. DOI: https://doi.org/10.1007/s00248-014-0536-9
Halpern M, Senderovich Y, Snir S, 2007. Rheinheimera chironomi sp. nov., isolated from a chironomid (Diptera; Chironomidae) egg mass. Int. J. Syst. Evol. Microbiol. 57:1872-1875. DOI: https://doi.org/10.1099/ijs.0.64927-0
Hamidou Soumana I, Linz B, Harvill ET, 2017. Environmental origin of the genus Bordetella. Front. Microbiol. 8:28. DOI: https://doi.org/10.3389/fmicb.2017.00028
Herrera LM, García-Laviña CX, Marizcurrena JJ, Volonterio O, León RP de, Castro-Sowinski S, 2017. Hydrolytic enzyme-producing microbes in the Antarctic oligochaete Grania sp. (Annelida). Polar Biol. 40:947–953. DOI: https://doi.org/10.1007/s00300-016-2012-0
Higgins RP, Thiel H, 1988. Introduction to the study of meiofauna. Washington DC, Smithsonian Institution Press: 488 pp.
Hong B, Ba Y, Niu L, Lou F, Zhang Z, Liu H, Pan Y, Zhao Y, 2018. A comprehensive research on antibiotic resistance genes in microbiota of aquatic animals. Front. Microbiol. 9:1617. DOI: https://doi.org/10.3389/fmicb.2018.01617
Horppila J, Ruuhijarvi J, Rask M, Karppinen C, Nyberg K, Olin M, 2000. Seasonal changes in the diets and relative abundances of perch and roach in the littoral and pelagic zones of a large lake. J. Fish Biol. 56:51-72. DOI: https://doi.org/10.1111/j.1095-8649.2000.tb02086.x
Howard A, O’Donoghue M, Feeney A, Sleator RD, 2012. Acinetobacter baumannii: An emerging opportunistic pathogen. Virulence 3:243–250. DOI: https://doi.org/10.4161/viru.19700
Hurtado L, Miranda CD, Rojas R, Godoy FA, Añazco MA, Romero J, 2020. Live feeds used in the larval culture of red cusk eel, Genypterus chilensis, carry high levels of antimicrobial-resistant bacteria and antibiotic-resistance genes (ARGs). Animals 10:505. DOI: https://doi.org/10.3390/ani10030505
Janda JM, Abbott SL, 2010. The genus Aeromonas: Taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev. 23:35–73. DOI: https://doi.org/10.1128/CMR.00039-09
Jarett J, Fiore C, Mazel C, Lesser M, 2013. Fluorescent epibiotic microbial community on the carapace of a Bahamian ostracod. Arch. Microbiol. 195:595–604. DOI: https://doi.org/10.1007/s00203-013-0911-9
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. DOI: 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. DOI: https://doi.org/10.1016/j.scitotenv.2018.06.149
Kalatzis PG, Bastías R, Kokkari C, Katharios P, 2016. Isolation and characterization of two lytic bacteriophages, φSt2 and φGrn1; Phage therapy application for biological control of Vibrio alginolyticus in aquaculture live feeds. PLoS One 11:e0151101. DOI: https://doi.org/10.1371/journal.pone.0151101
Kathol M, Fischer H, Weitere M, 2011. Contribution of biofilm-dwelling consumers to pelagic-benthic coupling in a large river: Pelagic-benthic coupling by biofilms. Freshwater Biol. 56:1160–1172. DOI: https://doi.org/10.1111/j.1365-2427.2010.02561.x
Kornijów R, 1997. The impact of predation by perch on the size-structure of Chironomus larvae - the role of vertical distribution of the prey in the bottom sediments, and habitat complexity, p. 207–213. In: L. Kufel, A. Prejs and J.I. Rybak (eds.), Shallow lakes ’95: Trophic cascades in shallow freshwater and brackish lakes. Dordrecht, Springer. DOI: https://doi.org/10.1007/978-94-011-5648-6_22
Kos J, Brmež M, Markić M, Sipos L, 2020. The mortality of nematodes in drinking water in the presence of ozone, chlorine dioxide, and chlorine. Ozone-Sci. Eng. 42:120–127. DOI: https://doi.org/10.1080/01919512.2019.1605877
Laviad S, Halpern M, 2016. Chironomids’ Relationship with Aeromonas Species. Front. Microbiol. 7:736. DOI: https://doi.org/10.3389/fmicb.2016.00736
Leonard AFC, Zhang L, Balfour AJ, Garside R, Hawkey PM, Murray AK, Ukoumunne OC, Gaze WH, 2018. Exposure to and colonisation by antibiotic-resistant E. coli in UK coastal water users: Environmental surveillance, exposure assessment, and epidemiological study (Beach Bum Survey). Environ. Int. 114:326-333. DOI: https://doi.org/10.1016/j.envint.2017.11.003
Loch TP, Faisal M, 2015. Emerging flavobacterial infections in fish: A review. J. Adv. Res. 6:283–300. DOI: https://doi.org/10.1016/j.jare.2014.10.009
Macke E, Callens M, De Meester L, Decaestecker E, 2017. Host-genotype dependent gut microbiota drives zooplankton tolerance to toxic cyanobacteria. Nat. Commun. 8:1608. DOI: https://doi.org/10.1038/s41467-017-01714-x
MacLean RC, Millan AS, 2019. The evolution of antibiotic resistance. Science 365:1082-1083. DOI: https://doi.org/10.1126/science.aax3879
Majdi N, Schmid-Araya JM, Traunspurger W, 2020. Preface: Patterns and processes of meiofauna in freshwater ecosystems. Hydrobiologia 847:2587–2595. DOI: https://doi.org/10.1007/s10750-020-04301-2
Majdi N, Threis I, Traunspurger W, 2017. It's the little things that count: Meiofaunal density and production in the sediment of two headwater streams. Limnol. Oceanogr. 62:151-163. DOI: https://doi.org/10.1002/lno.10382
Marchesi JR, Ravel J, 2015. The vocabulary of microbiome research: a proposal. Microbiome 3:31. DOI: https://doi.org/10.1186/s40168-015-0094-5
Marti E, Variatza E, Balcazar JL, 2014. The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol. 22:36–41. DOI: https://doi.org/10.1016/j.tim.2013.11.001
Martins MJF, Vandekerkhove J, Mezquita F, Schmit O, Rueda J, Rossetti G, Namiotko T, 2009. Dynamics of sexual and parthenogenetic populations of Eucypris virens (Crustacea: Ostracoda) in three temporary ponds. Hydrobiologia 636:219–232. DOI: https://doi.org/10.1007/s10750-009-9952-0
Martínez A, Eckert EM, Artois T, Careddu G, Casu M, Curini Galletti M, Gazale V, Gobert S, Ivanenko VN, Jondelius U, Marzano M, Pesole G, Zanello A, Todaro MA, Fontaneto D, 2020. Human access impacts biodiversity of microscopic animals in sandy beaches. Commun. Biol. 3:175. DOI: https://doi.org/10.1038/s42003-020-0912-6
Moore BC, Martinez E, Gay JM, Rice DH, 2003. Survival of Salmonella enterica in freshwater and sediments and transmission by the aquatic midge Chironomus tentans (Chironomidae: Diptera). Appl. Environ. Microbiol. 69:4556–4560. DOI: https://doi.org/10.1128/AEM.69.8.4556-4560.2003
Mughini-Gras L, Dorado-García A, Duijkeren E van, Bunt G van den, Dierikx CM, Bonten MJM, Bootsma MCJ, Schmitt H, Hald T, Evers EG, Koeijer A de, Pelt W van, et al., 2019. Attributable sources of community-acquired carriage of Escherichia coli containing β-lactam antibiotic resistance genes: a population-based modelling study. Lancet Planet. Health 3:e357-e369. DOI: https://doi.org/10.1016/S2542-5196(19)30130-5
Näslund J, Nascimento FJ, Gunnarsson JS, 2010. Meiofauna reduces bacterial mineralization of naphthalene in marine sediment. ISME J. 4:1421-1430. DOI: https://doi.org/10.1038/ismej.2010.63
Nasri A, Allouche M, Hannachi A, Harrath AH, Aldahmash W, Alwasel S, Mahmoudi E, Beyrem H, Boufahja F, 2020. Restructuring of a meiobenthic assemblage after sediment contamination with an antibacterial compound: Case study of ciprofloxacin. Ecotoxicol. Environ. Saf. 205:111084. DOI: https://doi.org/10.1016/j.ecoenv.2020.111084
Nematollahi A, Decostere A, Pasmans F, Haesebrouck F, 2003. Flavobacterium psychrophilum infections in salmonid fish. J. Fish Dis. 26:563–574. DOI: https://doi.org/10.1046/j.1365-2761.2003.00488.x
Neuenschwander SM, Pernthaler J, Posch T, Salcher MM, 2015. Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. Environ. Microbiol. 17:781-795. DOI: https://doi.org/10.1111/1462-2920.12520
Nnadozie CF, Odume ON, 2019. Freshwater environments as reservoirs of antibiotic resistant bacteria and their role in the dissemination of antibiotic resistance genes. Environ. Pollut. 254:113067. DOI: https://doi.org/10.1016/j.envpol.2019.113067
Oh M, Pruden A, Chen C, Heath LS, Xia K, Zhang L, 2018. MetaCompare: a computational pipeline for prioritizing environmental resistome risk. FEMS Microbiol. Ecol. 94:fiy079. DOI: https://doi.org/10.1093/femsec/fiy079
Olanrewaju TO, McCarron M, Dooley JSG, Arnscheidt J, 2019. Transfer of antibiotic resistance genes between Enterococcus faecalis strains in filter feeding zooplankton Daphnia magna and Daphnia pulex. Sci. Total Environ. 659:1168–1175. DOI: https://doi.org/10.1016/j.scitotenv.2018.12.314
Olmo C, Armengol X, Antón-Pardo M, Ortells R, 2016. The environmental and zooplankton community changes in restored ponds over 4 years. J. Plankton Res. 38:490–501. DOI: https://doi.org/10.1093/plankt/fbw021
Olszewski P, Bruhn-Olszewska B, Namiotko L, Sell J, Namiotko T, 2020. Co-cultured non-marine ostracods from a temporary wetland harbor host-specific microbiota of different metabolic profiles. Hydrobiologia 847:2503-2519. DOI: https://doi.org/10.1007/s10750-020-04269-z
O’Neill J, 2014. Antimicrobial resistance. Tackling a crisis for the health and wealth of nations. Available from: https://wellcomecollection.org/works/rdpck35v/items
Peerakietkhajorn S, Kato Y, Kasalický V, Matsuura T, Watanabe H, 2016. Betaproteobacteria Limnohabitans strains increase fecundity in the crustacean Daphnia magna: symbiotic relationship between major bacterioplankton and zooplankton in freshwater ecosystem. Environ. Microbiol. 18:2366-2374. DOI: https://doi.org/10.1111/1462-2920.12919
Philipsborn R, Ahmed SM, Brosi BJ, Levy K, 2016. Climatic drivers of diarrheagenic Escherichia coli incidence: A systematic review and meta-analysis. J. Infect. Dis. 214:6-15. DOI: https://doi.org/10.1093/infdis/jiw081
Pinto TK, Austen MCV, Warwick RM, Somerfield PJ, Esteves AM, Castro FJV, Fonseca-Genevois VG, Santos PJP, 2013. Nematode diversity in different microhabitats in a mangrove region. Mar. Ecol. 34:257-268. DOI: https://doi.org/10.1111/maec.12011
Prather CM, Pelini SL, Laws A, Rivest E, Woltz M, Bloch CP, Toro ID, Ho C-K, Kominoski J, Newbold TAS, Parsons S, Joern A, 2013. Invertebrates, ecosystem services and climate change. Biol. Rev. 88:327-348. DOI: https://doi.org/10.1111/brv.12002
Preiswerk D, Walser J-C, Ebert D, 2018. Temporal dynamics of microbiota before and after host death. ISME J. 12:2076-2085. DOI: https://doi.org/10.1038/s41396-018-0157-2
Ptatscheck C, Gehner S, Traunspurger W, 2020. Should we redefine meiofaunal organisms? The impact of mesh size on collection of meiofauna with special regard to nematodes. Aquat. Ecol. 54:1135-1143. DOI: https://doi.org/10.1007/s10452-020-09798-2
Ptatscheck C, Gansfort B, Traunspurger W, 2018. The extent of wind-mediated dispersal of small metazoans, focusing nematodes. Sci. Rep. 8:6814. DOI: https://doi.org/10.1038/s41598-018-24747-8
Pund RP, Theegarten D, 2008. [The importance of aeromonads as a human pathogen].[Article in German]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 51:569-576. DOI: https://doi.org/10.1007/s00103-008-0531-8
Qi W, Nong G, Preston JF, Ben-Ami F, Ebert D, 2009. Comparative metagenomics of Daphnia symbionts. BMC Genomics 10:172. DOI: https://doi.org/10.1186/1471-2164-10-172
Quinlan EL, Nietch CT, Blocksom K, Lazorchak JM, Batt AL, Griffiths R, Klemm DJ, 2011. temporal Dynamics of Periphyton Exposed to Tetracycline in Stream Mesocosms. Environ. Sci. Technol. 45:10684–10690. DOI: https://doi.org/10.1021/es202004k
Rhee SH, Pothoulakis C, Mayer EA, 2009. Principles and clinical implications of the brain–gut–enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 6:306–314. DOI: https://doi.org/10.1038/nrgastro.2009.35
Robinson TP, Bu DP, Carrique-Mas J, Fèvre EM, Gilbert M, Grace D, Hay SI, Jiwakanon J, Kakkar M, Kariuki S, Laxminarayan R, Lubroth J, Magnusson U, Thi Ngoc P, Van Boeckel TP, Woolhousep MEJ, 2016. Antibiotic resistance is the quintessential One Health issue. Trans. R. Soc. Trop. Med. Hyg. 110:377–380. DOI: https://doi.org/10.1093/trstmh/trw048
Rossi V, Albini D, Benassi G, Menozzi P, 2012. To rest in hydration: Hatching phenology of resting eggs of Heterocypris incongruens (Crustacea: Ostracoda). Fund. Appl. Limnol. 181:49–58. DOI: https://doi.org/10.1127/1863-9135/2012/0251
Sahandi J, Sorgeloos P, Xiao H, Wang X, Qi Z, Zheng Y, Tang X, 2019. The use of selected bacteria and yeasts to control Vibrio spp. in live food. Antibiotics 8:95. DOI: https://doi.org/10.3390/antibiotics8030095
Sathicq MB, Sabatino R, Corno G, Di Cesare A, 2021. Are microplastic particles a hotspot for the spread and the persistence of antibiotic resistance in aquatic systems? Environ. Pollut. 279:116896. DOI: https://doi.org/10.1016/j.envpol.2021.116896
Schmid PE, Tokeshi M, Schmid-Araya JM, 2000. Relation between population density and body size in stream communities. Science 289:1557-1560. DOI: https://doi.org/10.1126/science.289.5484.1557
Schmid-Araya JM, Schmid PE, Majdi N, Traunspurger W, 2020. Biomass and production of freshwater meiofauna: a review and a new allometric model. Hydrobiologia 847:2681-2703. DOI: https://doi.org/10.1007/s10750-020-04261-7
Schratzberger M, Ingels J, 2018. Meiofauna matters: The roles of meiofauna in benthic ecosystems. J. Exp. Mar. Biol. Ecol. 502:12-25.
Schmid-Araya JM, Schmid PE, 2000. Trophic relationships: integrating meiofauna into a realistic benthic food web. Freshwater Biol. 44:149-163. DOI: https://doi.org/10.1046/j.1365-2427.2000.00594.x
Schön I, Kamiya T, Van den Berghe T, Van den Broecke L, Martens K, 2019. Novel Cardinium strains in non-marine ostracod (Crustacea) hosts from natural populations. Mol. Phylogenet. Evol. 130:406–415. DOI: https://doi.org/10.1016/j.ympev.2018.09.008
Schratzberger M, Somerfield PJ, 2020. Effects of widespread human disturbances in the marine environment suggest a new agenda for meiofauna research is needed. Sci. Total Environ. 728:138435. DOI: https://doi.org/10.1016/j.scitotenv.2020.138435
Schratzberger M, Ingels J, 2018. Meiofauna matters: The roles of meiofauna in benthic ecosystems. J. Exp. Mar. Biol. Ecol. 502:12–25. DOI: https://doi.org/10.1016/j.jembe.2017.01.007
Schratzberger M, Warwick RM, 1999. Differential effects of various types of disturbances on the structure of nematode assemblages: an experimental approach. Marine Ecology Progress Series 181:227–236. DOI: https://doi.org/10.3354/meps181227
Senderovich Y, Gershtein Y, Halewa E, Halpern M, 2008. Vibrio cholerae and Aeromonas: do they share a mutual host? ISME J. 2:276–283. DOI: https://doi.org/10.1038/ismej.2007.114
Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E, 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl. Acad. Sci. 107:20051–20056. DOI: https://doi.org/10.1073/pnas.1009906107
Shin SC, Kim S-H, You H, Kim B, Kim AC, Lee K-A, Yoon J-H, Ryu J-H, Lee W-J, 2011. Drosophila Microbiome Modulates Host Developmental and Metabolic Homeostasis via Insulin Signaling. Science 334:670-674. DOI: https://doi.org/10.1126/science.1212782
Sison-Mangus MP, Mushegian AA, Ebert D, 2015. Water fleas require microbiota for survival, growth and reproduction. ISME J. 9:59-67. DOI: https://doi.org/10.1038/ismej.2014.116
Sommer F, Bäckhed F, 2013. The gut microbiota - masters of host development and physiology. Nat. Rev. Microbiol. 11:227-238. DOI: https://doi.org/10.1038/nrmicro2974
Stead TK, Schmid-Araya JM, Hildrew AG, 2005. Secondary production of a stream metazoan community: Does the meiofauna make a difference? Limnol. Oceanogr. 50:398–403. DOI: https://doi.org/10.4319/lo.2005.50.1.0398
Stratev D, Odeyemi OA, 2016. Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources: A mini-review. Journal of Infection and Public Health 9:535–544. DOI: https://doi.org/10.1016/j.jiph.2015.10.006
Suzuki S, Pruden A, Virta M, Zhang T, 2017. Editorial: Antibiotic resistance in aquatic systems. Front. Microbiol. 8:14. DOI: https://doi.org/10.3389/fmicb.2017.00014
Syrova E, Kohoutova L, Dolejska M, Papezikova I, Kutilova I, Cizek A, Navratil S, Minarova H, Palikova M, 2018. Antibiotic resistance and virulence factors in mesophilic Aeromonas spp. from Czech carp fisheries. J. Appl. Microbiol. 125:1702-1713. DOI: https://doi.org/10.1111/jam.14075
Tang K, 2005. Copepods as microbial hotspots in the ocean: effects of host feeding activities on attached bacteria. Aquat. Microb. Ecol. 38:31-40. DOI: https://doi.org/10.3354/ame038031
Tang K, Turk V, Grossart H, 2010. Linkage between crustacean zooplankton and aquatic bacteria. Aquat. Microb. Ecol. 61:261-277. DOI: https://doi.org/10.3354/ame01424
Tang KW, Dziallas C, Grossart H-P, 2011. Zooplankton and aggregates as refuge for aquatic bacteria: protection from UV, heat and ozone stresses used for water treatment. Environ. Microbiol. 13:378–390. DOI: https://doi.org/10.1111/j.1462-2920.2010.02335.x
Traunspurger W, Majdi N, 2017. Meiofauna, p. 273-295 In: F. Hauer and G. Lamberti (eds.), Methods in Stream Ecology. Amsterdam, Elsevier. DOI: https://doi.org/10.1016/B978-0-12-416558-8.00014-7
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI, 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031. DOI: https://doi.org/10.1038/nature05414
Vandekerkhove J, Martens K, Rossetti G, Mesquita-Joanes F, Namiotko T, 2013. Extreme tolerance to environmental stress of sexual and parthenogenetic resting eggs of Eucypris virens (Crustacea, Ostracoda). Freshwater Biol. 58:237–247. DOI: https://doi.org/10.1111/fwb.12051
Vayssier-Taussat M, Albina E, Citti C, Cosson JF, Jacques MA, Lebrun MH, Le Loir Y, Ogliastro M, Petit MA, Roumagnac P, Candresse T, 2014. Shifting the paradigm from pathogens to pathobiome: new concepts in the light of meta-omics. Front. Cell Infect. Microbiol. 5:4-29. DOI: https://doi.org/10.3389/fcimb.2014.00029
Waldor MK, Tyson G, Borenstein E, Ochman H, Moeller A, Finlay BB, Kong HH, Gordon JI, Nelson KE, Dabbagh K, Smith H, 2015. Where Next for Microbiome Research? PLoS Biol. 13:e1002050. DOI: https://doi.org/10.1371/journal.pbio.1002050
Xue X, Wang L, Xing H, Zhao Y, Li X, Wang G, Wang Z, 2021. Characteristics of phytoplankton-zooplankton communities and the roles in the transmission of antibiotic resistance genes under the pressure of river contamination. Sci. Total Environ. 780:146452. DOI: https://doi.org/10.1016/j.scitotenv.2021.146452
Zeppilli D, Sarrazin J, Leduc D, Arbizu PM, Fontaneto D, Fontanier C, Gooday AJ, Kristensen RM, Ivanenko VN, Sørensen MV, Vanreusel A, Thébault J, et al., 2015. Is the meiofauna a good indicator for climate change and anthropogenic impacts? Mar. Biodivers. 45:505–535. DOI: https://doi.org/10.1007/s12526-015-0359-z

Supporting Agencies

Cariplo Foundation (WARFARE project, grant n° 2018-0995), International Commission for the Protection of Italian-Swiss Waters (“INDAGINI LIMNOLOGICHE SUL LAGO MAGGIORE” program)

How to Cite

Sathicq, Maria Belen, Tomasa Sbaffi, Giulia Borgomaneiro, Andrea Di Cesare, and Raffaella Sabatino. 2021. “The Meiofauna As Neglected Carriers of Antibiotic Resistant and Pathogenic Bacteria in Freshwater Ecosystems”. Journal of Limnology 80 (3). https://doi.org/10.4081/jlimnol.2021.2054.

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