Anna E. Lindell, Anne Griesshammer, Lena Michaelis, Dimitrios Papagiannidis, Hannah Ochner, Stephan Kamrad, Rui Guan, Sonja Blasche, Leandro Ventimiglia, Bini Ramachandran, Hilal Ozgur, Aleksej Zelezniak, Nonantzin Beristain-Covarrubias, Juan Carlos Yam-Puc, Indra Roux, Leon P. Barron, Alexandra K. Richardson, Maria Guerra Martin, Vladimir Benes, Nobuhiro Morone, James Thaventhiran, Tanmay A.M. Bharat, Mikhail Savitski, Lisa Maier, Kiran Raosaheb Patil
{"title":"人体肠道细菌广泛积累全氟辛烷磺酸","authors":"Anna E. Lindell, Anne Griesshammer, Lena Michaelis, Dimitrios Papagiannidis, Hannah Ochner, Stephan Kamrad, Rui Guan, Sonja Blasche, Leandro Ventimiglia, Bini Ramachandran, Hilal Ozgur, Aleksej Zelezniak, Nonantzin Beristain-Covarrubias, Juan Carlos Yam-Puc, Indra Roux, Leon P. Barron, Alexandra K. Richardson, Maria Guerra Martin, Vladimir Benes, Nobuhiro Morone, James Thaventhiran, Tanmay A.M. Bharat, Mikhail Savitski, Lisa Maier, Kiran Raosaheb Patil","doi":"10.1101/2024.09.17.613493","DOIUrl":null,"url":null,"abstract":"Per- and polyfluoroalkyl Substances (PFAS) - the so-called 'forever chemicals' - are a major cause of environmental and health concern due to their toxicity and long-term persistence[1,2]. Yet, no efficient mechanisms for their removal have been identified. Here we report bioaccumulation of PFAS by several gut bacterial species over a wide range of concentrations from nanomolar up to 500 μM. For bioaccumulating <em>Bacteroides uniformis</em>, a highly prevalent species, we estimate intracellular PFAS concentration in the mM range - above that of most native metabolites. Despite this high bioaccumulation, <em>B. uniformis</em> cells could grow appreciably up to 250 μM perfluorononanoic acid (PFNA) exposure. <em>Escherichia coli</em>, which accumulated PFAS to a much lesser extent, substantially increased PFAS bioaccumulation when lacking TolC efflux pump indicating trans-membrane transport in PFAS bioaccumulation. Electron microscopy and cryogenic Focused Ion Beam-Secondary Ion Mass-spectrometry revealed distinct morphological changes and intracellular localisation of PFNA aggregates. Bioaccumulation of PFAS and transmembrane transport is also evident in proteomics, metabolomics, thermal proteome profiling, and mutations following adaptive laboratory evolution. In an in vivo context, mice colonized with human gut bacteria showed, compared to germ-free controls or those colonized with low-bioaccumulating bacteria, higher PFNA levels in excreted feces. As the gut microbiota is a critical interface between exposure and human body, our results have implications for understanding and utilizing microbial contribution to PFAS clearance.","PeriodicalId":501357,"journal":{"name":"bioRxiv - Microbiology","volume":"54 48 1","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Extensive PFAS accumulation by human gut bacteria\",\"authors\":\"Anna E. Lindell, Anne Griesshammer, Lena Michaelis, Dimitrios Papagiannidis, Hannah Ochner, Stephan Kamrad, Rui Guan, Sonja Blasche, Leandro Ventimiglia, Bini Ramachandran, Hilal Ozgur, Aleksej Zelezniak, Nonantzin Beristain-Covarrubias, Juan Carlos Yam-Puc, Indra Roux, Leon P. Barron, Alexandra K. Richardson, Maria Guerra Martin, Vladimir Benes, Nobuhiro Morone, James Thaventhiran, Tanmay A.M. Bharat, Mikhail Savitski, Lisa Maier, Kiran Raosaheb Patil\",\"doi\":\"10.1101/2024.09.17.613493\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Per- and polyfluoroalkyl Substances (PFAS) - the so-called 'forever chemicals' - are a major cause of environmental and health concern due to their toxicity and long-term persistence[1,2]. Yet, no efficient mechanisms for their removal have been identified. Here we report bioaccumulation of PFAS by several gut bacterial species over a wide range of concentrations from nanomolar up to 500 μM. For bioaccumulating <em>Bacteroides uniformis</em>, a highly prevalent species, we estimate intracellular PFAS concentration in the mM range - above that of most native metabolites. Despite this high bioaccumulation, <em>B. uniformis</em> cells could grow appreciably up to 250 μM perfluorononanoic acid (PFNA) exposure. <em>Escherichia coli</em>, which accumulated PFAS to a much lesser extent, substantially increased PFAS bioaccumulation when lacking TolC efflux pump indicating trans-membrane transport in PFAS bioaccumulation. Electron microscopy and cryogenic Focused Ion Beam-Secondary Ion Mass-spectrometry revealed distinct morphological changes and intracellular localisation of PFNA aggregates. Bioaccumulation of PFAS and transmembrane transport is also evident in proteomics, metabolomics, thermal proteome profiling, and mutations following adaptive laboratory evolution. In an in vivo context, mice colonized with human gut bacteria showed, compared to germ-free controls or those colonized with low-bioaccumulating bacteria, higher PFNA levels in excreted feces. As the gut microbiota is a critical interface between exposure and human body, our results have implications for understanding and utilizing microbial contribution to PFAS clearance.\",\"PeriodicalId\":501357,\"journal\":{\"name\":\"bioRxiv - Microbiology\",\"volume\":\"54 48 1\",\"pages\":\"\"},\"PeriodicalIF\":0.0000,\"publicationDate\":\"2024-09-17\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"bioRxiv - Microbiology\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1101/2024.09.17.613493\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"\",\"JCRName\":\"\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"bioRxiv - Microbiology","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1101/2024.09.17.613493","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
Per- and polyfluoroalkyl Substances (PFAS) - the so-called 'forever chemicals' - are a major cause of environmental and health concern due to their toxicity and long-term persistence[1,2]. Yet, no efficient mechanisms for their removal have been identified. Here we report bioaccumulation of PFAS by several gut bacterial species over a wide range of concentrations from nanomolar up to 500 μM. For bioaccumulating Bacteroides uniformis, a highly prevalent species, we estimate intracellular PFAS concentration in the mM range - above that of most native metabolites. Despite this high bioaccumulation, B. uniformis cells could grow appreciably up to 250 μM perfluorononanoic acid (PFNA) exposure. Escherichia coli, which accumulated PFAS to a much lesser extent, substantially increased PFAS bioaccumulation when lacking TolC efflux pump indicating trans-membrane transport in PFAS bioaccumulation. Electron microscopy and cryogenic Focused Ion Beam-Secondary Ion Mass-spectrometry revealed distinct morphological changes and intracellular localisation of PFNA aggregates. Bioaccumulation of PFAS and transmembrane transport is also evident in proteomics, metabolomics, thermal proteome profiling, and mutations following adaptive laboratory evolution. In an in vivo context, mice colonized with human gut bacteria showed, compared to germ-free controls or those colonized with low-bioaccumulating bacteria, higher PFNA levels in excreted feces. As the gut microbiota is a critical interface between exposure and human body, our results have implications for understanding and utilizing microbial contribution to PFAS clearance.