{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T00:12:01Z","timestamp":1785715921272,"version":"3.56.0"},"reference-count":82,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,3,15]],"date-time":"2022-03-15T00:00:00Z","timestamp":1647302400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000015","name":"U.S. Department of Energy","doi-asserted-by":"publisher","award":["LANLF59T"],"award-info":[{"award-number":["LANLF59T"]}],"id":[{"id":"10.13039\/100000015","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000928","name":"Welch Foundation","doi-asserted-by":"publisher","award":["E\u22122011-20190330"],"award-info":[{"award-number":["E\u22122011-20190330"]}],"id":[{"id":"10.13039\/100000928","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["2125480"],"award-info":[{"award-number":["2125480"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["2125104"],"award-info":[{"award-number":["2125104"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["2125298"],"award-info":[{"award-number":["2125298"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Most studies on metal removal or tolerance by fungi or bacteria focus on single isolates, without taking into consideration that some fungi in nature may be colonized by endobacteria. To address this knowledge gap, we investigated the tolerance and removal of diverse metals with two fungal species: <jats:italic>Linnemannia elongata<\/jats:italic> containing Burkholderia-related endobacteria and <jats:italic>Benniella erionia<\/jats:italic> containing Mollicute-related endobacteria. Isogenic lines of both species were generated with antibiotic treatments to remove their respective endobacteria. Experiments involved comparing the isogenic lines and wild type fungi in relation to the minimum inhibitory concentration for the metals, the fungal ability to remove these different metals <jats:italic>via<\/jats:italic> atomic adsorption spectroscopy, and the interaction of the metals with specific functional groups of the fungi and fungi-bacteria to determine the role of the bacteria <jats:italic>via<\/jats:italic> attenuated total reflection fourier transformed infrared (ATR-FTIR). Finally, we determined the influence of different metal concentrations, associated with moderate and high fungal growth inhibition, on the presence of the endobacteria inside the fungal mycelium <jats:italic>via<\/jats:italic> quantitative real-time PCR. Results showed that the presence of the endosymbiont increased <jats:italic>B. erionia<\/jats:italic> resistance to Mn<jats:sup>2+<\/jats:sup> and increased the removal of Fe<jats:sup>2+<\/jats:sup> compared to isogenic lines. The absence of the endosymbiont in <jats:italic>L. elongata<\/jats:italic> increased the fungal resistance toward Fe<jats:sup>2+<\/jats:sup> and improved the removal of Fe<jats:sup>2+<\/jats:sup>. Furthermore, when the bacterial endosymbiont was present in <jats:italic>L. elongata<\/jats:italic>, a decrease in the fungal resistance to Ca<jats:sup>2+<\/jats:sup>, Fe<jats:sup>2+<\/jats:sup>, and Cr<jats:sup>6+<\/jats:sup>was noticeable. In the ATR-FTIR analysis, we determined that C-H and C = O were the major functional groups affected by the presence of Cu<jats:sup>2+<\/jats:sup>, Mn<jats:sup>2+<\/jats:sup>, and Fe<jats:sup>2+<\/jats:sup> for <jats:italic>L. elongata<\/jats:italic> and in the presence of Cu<jats:sup>2+<\/jats:sup> and Ca<jats:sup>2+<\/jats:sup> for <jats:italic>B. eronia<\/jats:italic>. It is noteworthy that the highest concentration of Pb<jats:sup>2+<\/jats:sup> led to the loss of endobacteria in both <jats:italic>L. elongata<\/jats:italic> and <jats:italic>B. eronia<\/jats:italic>, while the other metals generally increased the concentration of endosymbionts inside the fungal mycelium. From these results, we concluded that bacterial endosymbionts of fungi can play a fundamental role in fungal resistance to metals. This study provides the first step toward a greater understanding of symbiotic interactions between bacteria and fungi in relation to metal tolerance and remediation.<\/jats:p>","DOI":"10.3389\/fmicb.2022.822541","type":"journal-article","created":{"date-parts":[[2023,1,6]],"date-time":"2023-01-06T22:26:17Z","timestamp":1673043977000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":14,"title":["Effect of Endosymbiotic Bacteria on Fungal Resistance Toward Heavy Metals"],"prefix":"10.3389","volume":"13","author":[{"given":"Simone","family":"Lupini","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janire","family":"Pe\u00f1a-Bahamonde","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gregory","family":"Bonito","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Debora F.","family":"Rodrigues","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,3,15]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/s0300-483x(98)00134-6","article-title":"Pb2+ promotes lipid oxidation and alterations in membrane physical properties.","volume":"132","author":"Adonaylo","year":"1999","journal-title":"Toxicology"},{"key":"B2","doi-asserted-by":"publisher","first-page":"13541","DOI":"10.1074\/jbc.R111.312181","article-title":"Battles with iron: manganese in oxidative stress protection.","volume":"287","author":"Aguirre","year":"2012","journal-title":"J. Biol. Chem."},{"key":"B3","first-page":"123","article-title":"Heavy metal biosorption potential of Aspergillus and Rhizopus sp. isolated from wastewater treated soil.","volume":"9","author":"Ahmad","year":"2005","journal-title":"J. Appl. Sci. Environ."},{"key":"B4","doi-asserted-by":"publisher","first-page":"1919","DOI":"10.1128\/aem.56.6.1919-1925.1990","article-title":"Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations.","volume":"56","author":"Amann","year":"1990","journal-title":"Appl. Environ. Microbiol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1007\/978-3-642-02436-8_2","article-title":"Definition of \u201cheavy metals\u201d and their role in biological systems.","volume":"19","author":"Appenroth","year":"2010","journal-title":"Soil Heavy Metals"},{"key":"B6","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1016\/j.biortech.2011.05.092","article-title":"Interactions of heavy metals with white-rot fungi.","volume":"32","author":"Baldrian","year":"2003","journal-title":"Enzyme Microb. Technol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.pbi.2019.10.010","article-title":"Symbiotic bacteria of plant-associated fungi: friends or foes?","volume":"56","author":"Bast\u00edas","year":"2020","journal-title":"Curr. Opin. Plant Biol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1007\/BF02014282","article-title":"Influence of extracellular polysaccharides on the toxicity of copper and cadmium toward Klebsiella aerogenes.","volume":"4","author":"Bitton","year":"1977","journal-title":"Microb. Ecol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1221","DOI":"10.1016\/j.saa.2010.10.025","article-title":"Classification of the biological material with use of FTIR spectroscopy and statistical analysis.","volume":"78","author":"Bombalska","year":"2011","journal-title":"Spectrochim. Acta A Mol. Biomol. Spectrosc."},{"key":"B10","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1016\/s0043-1354(97)00273-x","article-title":"The removal and recovery of cadmium from dilute aqueous solutions by biosorption and electrolysis at laboratory scale.","volume":"32","author":"Butter","year":"1998","journal-title":"Water Res."},{"key":"B11","doi-asserted-by":"publisher","first-page":"5308","DOI":"10.1128\/AEM.00324-07","article-title":"The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation.","volume":"73","author":"Caballero-Mellado","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"35602","DOI":"10.1007\/s11356-019-04844-5","article-title":"Fungi as potential tool for polluted port sediment remediation.","volume":"26","author":"Cecchi","year":"2019","journal-title":"Environ. Sci. Pollut. Res."},{"key":"B13","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1111\/j.1574-6976.1994.tb00083.x","article-title":"Copper resistance mechanisms in bacteria and fungi.","volume":"14","author":"Cervantes","year":"1994","journal-title":"FEMS Microbiol. Rev."},{"key":"B14","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1016\/j.jhazmat.2018.08.077","article-title":"Mechanisms for metal removal established via electron microscopy and spectroscopy: a case study on metal tolerant fungi Penicillium simplicissimum.","volume":"362","author":"Chen","year":"2019","journal-title":"J. Hazardous Mater."},{"key":"B15","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1080\/01904160009382068","article-title":"Mineral acquisition by arbuscular mycorrhizal plants.","volume":"23","author":"Clark","year":"2000","journal-title":"J. Plant Nutr."},{"key":"B16","doi-asserted-by":"publisher","first-page":"33388","DOI":"10.1074\/jbc.M004611200","article-title":"The family of SMF metal ion transporters in yeast cells.","volume":"275","author":"Cohen","year":"2000","journal-title":"J. Biol. Chem."},{"key":"B17","first-page":"89","article-title":"Biological treatment of industrial liquid effluent in copper production industry.","volume":"18","author":"Cortes","year":"2003","journal-title":"Tecbahia Rev. Baiana Tecnol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1743","DOI":"10.1038\/s41396-018-0053-9","article-title":"Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle.","volume":"12","author":"Desir\u00f2","year":"2018","journal-title":"ISME J."},{"key":"B19","doi-asserted-by":"publisher","first-page":"467","DOI":"10.1080\/09593330.2011.572922","article-title":"Fungal biosorption\u2013an alternative to meet the challenges of heavy metal pollution in aqueous solutions.","volume":"32","author":"Dhankhar","year":"2011","journal-title":"Environ. Technol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1016\/j.jhazmat.2014.07.016","article-title":"The synergism of temperature, pH and growth phases on heavy metal biosorption by two environmental isolates.","volume":"279","author":"Fan","year":"2014","journal-title":"J. Hazardous Mater."},{"key":"B21","doi-asserted-by":"publisher","first-page":"3515","DOI":"10.1007\/s11356-013-2324-3","article-title":"Energy-dependent uptake of benzo [a] pyrene and its cytoskeleton-dependent intracellular transport by the telluric fungus Fusarium solani.","volume":"21","author":"Fayeulle","year":"2014","journal-title":"Environ. Sci. Pollut. Res."},{"key":"B22","doi-asserted-by":"publisher","first-page":"782","DOI":"10.1016\/j.chemphyslip.2011.09.006","article-title":"Oxidative changes of lipids monitored by MALDI MS.","volume":"164","author":"Fuchs","year":"2011","journal-title":"Chem. Phys. Lipids"},{"key":"B23","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1007\/978-1-4899-0981-7_28","article-title":"Interactions of fungi with toxic metals","author":"Gadd","year":"1994","journal-title":"The Genus Aspergillus. Federation of European Microbiological Societies Symposium Series"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2016.01088","article-title":"Transition metal transport in plants and associated endosymbionts: arbuscular mycorrhizal fungi and rhizobia.","volume":"7","author":"Gonz\u00e1lez-Guerrero","year":"2016","journal-title":"Front. Plant Sci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/s43538-021-00011-y","article-title":"Study of Langmuir kinetics for removal of heavy metals by the fungal biomass.","volume":"87","author":"Gunjal","year":"2021","journal-title":"Proc. Indian Natl. Sci. Acad."},{"key":"B26","author":"Hanson","year":"2014","journal-title":"ChemoSpec: An R Package for the Chemometric Analysis of Spectroscopic Data. Package Version, 2.0-2."},{"key":"B27","author":"Hitchins","year":"1998","journal-title":"Bacteriological Analytical Manual."},{"key":"B28","doi-asserted-by":"publisher","first-page":"2971","DOI":"10.1128\/aem.63.8.2971-2976.1997","article-title":"Induction of lipid peroxidation during heavy metal stress in Saccharomyces cerevisiae and influence of plasma membrane fatty acid unsaturation.","volume":"63","author":"Howlett","year":"1997","journal-title":"Appl. Environ. Microbiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.fgb.2014.09.005","article-title":"Five vacuolar Ca2+ exchangers play different roles in calcineurin-dependent Ca2+\/Mn2+ tolerance, multistress responses and virulence of a filamentous entomopathogen.","volume":"73","author":"Hu","year":"2014","journal-title":"Fungal Genet. Biol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.chemosphere.2008.02.006","article-title":"Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil.","volume":"72","author":"Jiang","year":"2008","journal-title":"Chemosphere"},{"key":"B31","article-title":"Heavy metal pollution and use of microorganisms for bioremediation","author":"Johnson","year":"2016","journal-title":"Proceedings of the 2016 ATINER Conference on Environemnt"},{"key":"B32","doi-asserted-by":"publisher","first-page":"565","DOI":"10.7745\/KJSSF.2012.45.4.565","article-title":"Heavy metal tolerance of fungi isolated from contaminated soil.","volume":"45","author":"Joo","year":"2012","journal-title":"Korean J. Soil Sci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1235","DOI":"10.1111\/j.1365-2958.2011.07886.x","article-title":"Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in Aspergillus fumigatus.","volume":"82","author":"Juvvadi","year":"2011","journal-title":"Mol. Microbiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1007\/s10661-008-0657-z","article-title":"Pesticide pollution of river Ghaggar in Haryana, India.","volume":"160","author":"Kaushik","year":"2010","journal-title":"Environ. Monit. Assess."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1185","DOI":"10.1046\/j.1365-2958.2003.03368.x","article-title":"Molecular mechanisms of iron uptake in fungi.","volume":"47","author":"Kosman","year":"2003","journal-title":"Mol. Microbiol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1201\/9781003067221-1","article-title":"Transition metal ion uptake in yeasts and filamentous fungi","author":"Kosman","year":"2020","journal-title":"Metal Ions in Fungi"},{"key":"B37","doi-asserted-by":"publisher","first-page":"10375","DOI":"10.1007\/s11356-020-11491-8","article-title":"Mycoremediation of heavy metals: processes, mechanisms, and affecting factors.","volume":"28","author":"Kumar","year":"2021","journal-title":"Environ. Sci. Pollut. Res."},{"key":"B38","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1007\/s00253-007-1300-6","article-title":"Real-time PCR determination of rRNA gene copy number: absolute and relative quantification assays with Escherichia coli.","volume":"78","author":"Lee","year":"2008","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1038\/nrmicro3028","article-title":"Antimicrobial activity of metals: mechanisms, molecular targets and applications.","volume":"11","author":"Lemire","year":"2013","journal-title":"Nat. Rev. Microbiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1016\/j.phytochem.2016.01.002","article-title":"Arbuscular mycorrhizal fungal responses to abiotic stresses: a review.","volume":"123","author":"Lenoir","year":"2016","journal-title":"Phytochemistry"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1041","DOI":"10.1111\/1462-2920.13605","article-title":"Integrated proteomics and metabolomics suggests symbiotic metabolism and multimodal regulation in a fungal-endobacterial system.","volume":"19","author":"Li","year":"2017","journal-title":"Environ. Microbiol."},{"key":"B42","first-page":"227","article-title":"Cadmium absorption and its effects on growth and mycelial morphology of the basidiomycete fungus, Schizophyllum commune.","volume":"72","author":"Lilly","year":"1992","journal-title":"Microbios"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2013.00091","article-title":"Manganese acquisition and homeostasis at the host-pathogen interface.","volume":"3","author":"Lisher","year":"2013","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B44","author":"Lucas","year":"2006","journal-title":"Another Multidimensional Analysis Package Version 0.8-18."},{"key":"B45","first-page":"443","article-title":"Effects of Mg2+, Fe3+, Mn2+ and Cu2+ ions on lipid accumulation by Cunninghamella bainieri 2A1.","volume":"43","author":"Manikan","year":"2014","journal-title":"Sains Malaysiana"},{"key":"B46","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1021\/acs.est.7b04131","article-title":"Relationship of biodiversity with heavy metal tolerance and sorption capacity: a meta-analysis approach.","volume":"52","author":"Mejias Carpio","year":"2018","journal-title":"Environ. Sci. Technol."},{"key":"B47","author":"Mix","year":"2011","journal-title":"Power SYBR Green RT-PCR Reagents Kit User Guide."},{"key":"B48","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1271\/bbb.60495","article-title":"Physiological roles of calcineurin in Saccharomyces cerevisiae with special emphasis on its roles in G2\/M cell-cycle regulation.","volume":"71","author":"Miyakawa","year":"2007","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"B49","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1038\/s41564-019-0383-z","article-title":"Genome mining identifies cepacin as a plant-protective metabolite of the biopesticidal bacterium Burkholderia ambifaria.","volume":"4","author":"Mullins","year":"2019","journal-title":"Nat. Microbiol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1007\/978-1-4615-5873-6_21","article-title":"Role of Ca++\/calmodulin binding proteins in Aspergillus nidulans cell cycle regulation.","volume":"2","author":"Nanthakumar","year":"1996","journal-title":"Prog. Cell Cycle Res."},{"key":"B51","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/j.gexplo.2007.04.011","article-title":"Abandoned mine sites as a source of contamination by heavy metals: a case study in a semi-arid zone.","volume":"96","author":"Navarro","year":"2008","journal-title":"J. Geochem. Explorat."},{"key":"B52","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1111\/j.1574-6976.1997.tb00347.x","article-title":"Classification of all putative permeases and other membrane plurispanners of the major facilitator superfamily encoded by the complete genome of Saccharomyces cerevisiae.","volume":"21","author":"Nelissen","year":"1997","journal-title":"FEMS Microbiol. Rev."},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1016\/j.chemosphere.2021.133474","article-title":"Sustainable biochar: a facile strategy for soil and environmental restoration, energygeneration, mitigation of global climate change and circular bioeconomy.","volume":"293","author":"Neogi","year":"2021","journal-title":"Chemosphere"},{"key":"B54","doi-asserted-by":"publisher","first-page":"160","DOI":"10.1039\/C6EN00442C","article-title":"Acute toxicity of graphene nanoplatelets on biological wastewater treatment process.","volume":"4","author":"Nguyen","year":"2017","journal-title":"Environ. Sci. Nano"},{"key":"B55","doi-asserted-by":"crossref","first-page":"2079","DOI":"10.1016\/S0021-9258(19)69736-X","article-title":"Active transport of basic amino acids driven by a proton motive force in vacuolar membrane vesicles of Saccharomyces cerevisiae.","volume":"256","author":"Ohsumi","year":"1981","journal-title":"J. Biol. Chem."},{"key":"B56","doi-asserted-by":"publisher","DOI":"10.1155\/2015\/245607","article-title":"Application of FTIR-ATR spectroscopy to determine the extent of lipid peroxidation in plasma during haemodialysis.","volume":"2015","author":"Oleszko","year":"2015","journal-title":"BioMed Res. Int."},{"key":"B57","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/j.mam.2004.02.012","article-title":"Metals in neurodegeneration: involvement of oxidants and oxidant-sensitive transcription factors.","volume":"25","author":"Oteiza","year":"2004","journal-title":"Mol. Aspects Med."},{"key":"B58","doi-asserted-by":"publisher","first-page":"1356","DOI":"10.1016\/j.chemosphere.2005.02.020","article-title":"Studies on hexavalent chromium biosorption by chemically-treated biomass of Ecklonia sp.","volume":"60","author":"Park","year":"2005","journal-title":"Chemosphere"},{"key":"B59","doi-asserted-by":"publisher","first-page":"1234","DOI":"10.1016\/j.jclepro.2017.11.061","article-title":"New insight into effective biosorption of lead from aqueous solution using Ralstonia solanacearum: characterization and mechanism studies.","volume":"174","author":"Pugazhendhi","year":"2018","journal-title":"J. Clean. Product."},{"key":"B60","doi-asserted-by":"publisher","DOI":"10.1016\/j.envpol.2019.113777","article-title":"The improved methods of heavy metals removal by biosorbents: a review.","volume":"258","author":"Qin","year":"2020","journal-title":"Environ. Pollut."},{"key":"B61","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/0025-326X(95)00116-5","article-title":"Biomonitoring of heavy metal availability in the marine environment.","volume":"31","author":"Rainbow","year":"1995","journal-title":"Mar. Pollut. Bull."},{"key":"B62","first-page":"681","author":"Rao","year":"1963","journal-title":"Chemical Applications of Infrared Spectroscopy."},{"key":"B63","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1007\/s00204-009-0487-y","article-title":"The involvement of transition metal ions on iron-dependent lipid peroxidation.","volume":"84","author":"Repetto","year":"2010","journal-title":"Arch. Toxicol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s42003-021-02693-y","article-title":"Widespread bacterial diversity within the bacteriome of fungi.","volume":"4","author":"Robinson","year":"2021","journal-title":"Commun. Biol."},{"key":"B65","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1111\/j.1758-2229.2012.00372.x","article-title":"The genetic basis of cadmium resistance of B urkholderia cenocepacia.","volume":"4","author":"Schwager","year":"2012","journal-title":"Environ. Microbiol. Rep."},{"key":"B66","doi-asserted-by":"publisher","first-page":"321","DOI":"10.17221\/4131-PSE","article-title":"Effects of heavy metal concentrations on biological activity of soil micro-organisms.","volume":"49","author":"Smejkalova","year":"2003","journal-title":"Plant Soil Environ. Microbiol."},{"key":"B67","author":"Solomons","year":"2016","journal-title":"Organic Chemistry."},{"key":"B68","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1016\/0891-5849(94)00159-h","article-title":"Oxidative mechanisms in the toxicity of metal ions.","volume":"18","author":"Stohs","year":"1995","journal-title":"Free Radic. Biol. Med."},{"key":"B69","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1016\/j.tim.2005.07.009","article-title":"Geomicrobiology of manganese (II) oxidation.","volume":"13","author":"Tebo","year":"2005","journal-title":"Trends Microbiol."},{"key":"B70","doi-asserted-by":"publisher","first-page":"271","DOI":"10.2113\/gsecongeo.59.2.271","article-title":"Syngenesis of sulfide ores; sulfate-reducing bacteria and copper toxicity.","volume":"59","author":"Temple","year":"1964","journal-title":"Econ. Geol."},{"key":"B71","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1007\/978-3-030-54422-5_8","article-title":"Role of fungi in bioremediation and environmental sustainability","author":"Tomer","year":"2021","journal-title":"Mycoremediation and Environmental Sustainability. Fungal Biology"},{"key":"B72","first-page":"69","article-title":"Genetic and molecular biology of metal tolerance in fungi","author":"Tomsett","year":"1993","journal-title":"Stress Tolerance of Fungi"},{"key":"B73","doi-asserted-by":"publisher","first-page":"2964","DOI":"10.1111\/1462-2920.13669","article-title":"Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens.","volume":"19","author":"Uehling","year":"2017","journal-title":"Environ. Microbiol."},{"key":"B74","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1007\/978-981-10-4059-7_27","article-title":"Role of bioremediation agents (bacteria, fungi, and algae) in alleviating heavy metal toxicity","author":"ul Hassan","year":"2017","journal-title":"Probiotics in Agroecosystem"},{"key":"B75","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.ecss.2007.06.007","article-title":"Detecting environmental change in estuaries: nutrient and heavy metal distributions in sediment cores in estuaries from the Gulf of Finland, Baltic Sea.","volume":"76","author":"Vaalgamaa","year":"2008","journal-title":"Estuarine Coast. Shelf Sci."},{"key":"B76","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1146\/annurev.bi.41.070172.000515","article-title":"Biochemical effects of mercury, cadmium, and lead.","volume":"41","author":"Vallee","year":"1972","journal-title":"Annu. Rev. Biochem."},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.1201\/9781420059496","author":"Varmuza","year":"2016","journal-title":"Introduction to Multivariate Statistical Analysis in Chemometrics."},{"key":"B78","doi-asserted-by":"publisher","first-page":"R555","DOI":"10.1016\/j.cub.2012.06.010","article-title":"Endosymbiosis.","volume":"22","author":"Wernegreen","year":"2012","journal-title":"Curr. Biol."},{"key":"B79","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1099\/00221287-133-3-727","article-title":"The uptake and cellular distribution of zinc in Saccharomyces cerevisiae.","volume":"133","author":"White","year":"1987","journal-title":"Microbiology"},{"key":"B80","doi-asserted-by":"publisher","first-page":"2557","DOI":"10.1016\/j.biortech.2006.09.051","article-title":"Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil.","volume":"98","author":"Zafar","year":"2007","journal-title":"Bioresour. Technol."},{"key":"B81","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-020-63813-y","article-title":"Multiple heavy metal tolerance and removal by an earthworm gut fungus Trichoderma brevicompactum QYCD-6.","volume":"10","author":"Zhang","year":"2020","journal-title":"Sci. Rep."},{"key":"B82","doi-asserted-by":"publisher","first-page":"381","DOI":"10.2174\/1570178043400668","article-title":"Human low-density lipoprotein oxidation: hypochlorous acid leads to the generation of lysophosphatidylcholines under acidic conditions.","volume":"1","author":"Zschornig","year":"2004","journal-title":"Lett. Organ. Chem."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.822541\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,6]],"date-time":"2023-01-06T22:26:29Z","timestamp":1673043989000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.822541\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,15]]},"references-count":82,"alternative-id":["10.3389\/fmicb.2022.822541"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2022.822541","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,15]]},"article-number":"822541"}}