Insights into the antibiotic resistance dissemination in a wastewater effluent microbiome: bacteria, viruses and vesicles matter
Summary Wastewater treatment plants effluents are considered as hotspots for the dispersion of antibiotic resistance genes (ARGs) into natural ecosystems. The bacterial resistome (ARG collection in a metagenome) analyses have provided clues on antibacterial resistance dynamics. However, viruses and...
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| Veröffentlicht in: | Environmental microbiology 2019-12, Vol.21 (12), p.4582-4596 |
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| creator | Maestre‐Carballa, Lucia Lluesma Gomez, Monica Angla Navarro, Andrea Garcia‐Heredia, Inmaculada Martinez‐Hernandez, Francisco Martinez‐Garcia, Manuel |
| description | Summary
Wastewater treatment plants effluents are considered as hotspots for the dispersion of antibiotic resistance genes (ARGs) into natural ecosystems. The bacterial resistome (ARG collection in a metagenome) analyses have provided clues on antibacterial resistance dynamics. However, viruses and vesicles are frequently ignored. Here, we addressed the bacterial, viral and vesicle resistomes from a representative wastewater effluent in natural conditions and amended with polymyxin, which is used as a last resort antibiotic. Metagenomics showed that the natural prokaryotic resistome was vast (9000 ARG hits/Gb metagenome) and diverse, while viral resistome was two orders of magnitude lower (50 ARG hits/Gb metagenome) suggesting that viruses rarely encoded ARGs. After polymyxin amendment, data showed no ARG enrichment – including to polymyxin – in the microbiome. Remarkably, microbiomes responded to polymyxin with a vast release of putative vesicles (threefold increase compared with the control), which might be used as 'traps' to decrease the antibiotic concentration. Intriguingly, although polymyxin resistance genes (PRGs) were rare in the microbiome (0.018% of total ARG found), in the viral and vesicle fractions, PRGs were more abundant (0.5%–0.8% of total ARG found). Our data suggest that vesicles could have a more active role in the context of transmission of antibiotic resistances. |
| doi_str_mv | 10.1111/1462-2920.14758 |
| format | Article |
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Wastewater treatment plants effluents are considered as hotspots for the dispersion of antibiotic resistance genes (ARGs) into natural ecosystems. The bacterial resistome (ARG collection in a metagenome) analyses have provided clues on antibacterial resistance dynamics. However, viruses and vesicles are frequently ignored. Here, we addressed the bacterial, viral and vesicle resistomes from a representative wastewater effluent in natural conditions and amended with polymyxin, which is used as a last resort antibiotic. Metagenomics showed that the natural prokaryotic resistome was vast (9000 ARG hits/Gb metagenome) and diverse, while viral resistome was two orders of magnitude lower (50 ARG hits/Gb metagenome) suggesting that viruses rarely encoded ARGs. After polymyxin amendment, data showed no ARG enrichment – including to polymyxin – in the microbiome. Remarkably, microbiomes responded to polymyxin with a vast release of putative vesicles (threefold increase compared with the control), which might be used as 'traps' to decrease the antibiotic concentration. Intriguingly, although polymyxin resistance genes (PRGs) were rare in the microbiome (0.018% of total ARG found), in the viral and vesicle fractions, PRGs were more abundant (0.5%–0.8% of total ARG found). Our data suggest that vesicles could have a more active role in the context of transmission of antibiotic resistances.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.14758</identifier><identifier>PMID: 31342640</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Anti-Bacterial Agents - pharmacology ; Antibiotic resistance ; Antibiotics ; Bacteria ; Bacteria - drug effects ; Bacteria - genetics ; Disease hot spots ; Disease resistance ; Drug resistance ; Drug Resistance, Microbial ; Effluents ; Extracellular Vesicles ; Genes ; Genes, Bacterial ; Metagenome ; Microbiomes ; Microbiota - drug effects ; Vesicles ; Viruses ; Viruses - genetics ; Waste Water - microbiology ; Wastewater treatment ; Wastewater treatment plants ; Water Microbiology</subject><ispartof>Environmental microbiology, 2019-12, Vol.21 (12), p.4582-4596</ispartof><rights>2019 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2019 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3718-26caf3465857bff9275c7998af175053f85cd40afb05743cc92839ac5775438a3</citedby><cites>FETCH-LOGICAL-c3718-26caf3465857bff9275c7998af175053f85cd40afb05743cc92839ac5775438a3</cites><orcidid>0000-0001-5056-1525</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.14758$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.14758$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,778,782,1414,27907,27908,45557,45558</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31342640$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Maestre‐Carballa, Lucia</creatorcontrib><creatorcontrib>Lluesma Gomez, Monica</creatorcontrib><creatorcontrib>Angla Navarro, Andrea</creatorcontrib><creatorcontrib>Garcia‐Heredia, Inmaculada</creatorcontrib><creatorcontrib>Martinez‐Hernandez, Francisco</creatorcontrib><creatorcontrib>Martinez‐Garcia, Manuel</creatorcontrib><title>Insights into the antibiotic resistance dissemination in a wastewater effluent microbiome: bacteria, viruses and vesicles matter</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Wastewater treatment plants effluents are considered as hotspots for the dispersion of antibiotic resistance genes (ARGs) into natural ecosystems. The bacterial resistome (ARG collection in a metagenome) analyses have provided clues on antibacterial resistance dynamics. However, viruses and vesicles are frequently ignored. Here, we addressed the bacterial, viral and vesicle resistomes from a representative wastewater effluent in natural conditions and amended with polymyxin, which is used as a last resort antibiotic. Metagenomics showed that the natural prokaryotic resistome was vast (9000 ARG hits/Gb metagenome) and diverse, while viral resistome was two orders of magnitude lower (50 ARG hits/Gb metagenome) suggesting that viruses rarely encoded ARGs. After polymyxin amendment, data showed no ARG enrichment – including to polymyxin – in the microbiome. Remarkably, microbiomes responded to polymyxin with a vast release of putative vesicles (threefold increase compared with the control), which might be used as 'traps' to decrease the antibiotic concentration. Intriguingly, although polymyxin resistance genes (PRGs) were rare in the microbiome (0.018% of total ARG found), in the viral and vesicle fractions, PRGs were more abundant (0.5%–0.8% of total ARG found). Our data suggest that vesicles could have a more active role in the context of transmission of antibiotic resistances.</description><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Bacteria - drug effects</subject><subject>Bacteria - genetics</subject><subject>Disease hot spots</subject><subject>Disease resistance</subject><subject>Drug resistance</subject><subject>Drug Resistance, Microbial</subject><subject>Effluents</subject><subject>Extracellular Vesicles</subject><subject>Genes</subject><subject>Genes, Bacterial</subject><subject>Metagenome</subject><subject>Microbiomes</subject><subject>Microbiota - drug effects</subject><subject>Vesicles</subject><subject>Viruses</subject><subject>Viruses - genetics</subject><subject>Waste Water - microbiology</subject><subject>Wastewater treatment</subject><subject>Wastewater treatment plants</subject><subject>Water Microbiology</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkTtvFDEQgC0EIiFQ0yFLNBQc8fO8S4eiACcF0UBtzfrGxNGuN9jenNLx05njwhU0uLHH883nxzD2Uop3ksa5NGu1Ur2i0DjbPWKnx53Hx7VUJ-xZrTdCSKedeMpOtNRGrY04Zb82uaYf163ylNvM2zVyyC0NaW4p8II11QY5IN-mWnFKGVqaM8Ec-A5qwx00LBxjHBfMjU8plJmqJ3zPBwiUS_CW36WyVKyk3vI7coaRggkapZ-zJxHGii8e5jP2_ePlt4vPq6uvnzYXH65WQTvZrdQ6QNRmbTvrhhh75Wxwfd9BlM4Kq2Nnw9YIiIOwzugQetXpHoJ1zhrdgT5jbw7e2zL_XLA2P6UacBwh47xUrxQdo43sFaGv_0Fv5qVkup1XWgkyCymIOj9Q9OBaC0Z_W9IE5d5L4ffN8fvv9_tW-D_NoYpXD95lmHB75P92gwB7AHZpxPv_-fzll81B_BvXnZna</recordid><startdate>201912</startdate><enddate>201912</enddate><creator>Maestre‐Carballa, Lucia</creator><creator>Lluesma Gomez, Monica</creator><creator>Angla Navarro, Andrea</creator><creator>Garcia‐Heredia, Inmaculada</creator><creator>Martinez‐Hernandez, Francisco</creator><creator>Martinez‐Garcia, Manuel</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5056-1525</orcidid></search><sort><creationdate>201912</creationdate><title>Insights into the antibiotic resistance dissemination in a wastewater effluent microbiome: bacteria, viruses and vesicles matter</title><author>Maestre‐Carballa, Lucia ; Lluesma Gomez, Monica ; Angla Navarro, Andrea ; Garcia‐Heredia, Inmaculada ; Martinez‐Hernandez, Francisco ; Martinez‐Garcia, Manuel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3718-26caf3465857bff9275c7998af175053f85cd40afb05743cc92839ac5775438a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Bacteria</topic><topic>Bacteria - drug effects</topic><topic>Bacteria - genetics</topic><topic>Disease hot spots</topic><topic>Disease resistance</topic><topic>Drug resistance</topic><topic>Drug Resistance, Microbial</topic><topic>Effluents</topic><topic>Extracellular Vesicles</topic><topic>Genes</topic><topic>Genes, Bacterial</topic><topic>Metagenome</topic><topic>Microbiomes</topic><topic>Microbiota - drug effects</topic><topic>Vesicles</topic><topic>Viruses</topic><topic>Viruses - genetics</topic><topic>Waste Water - microbiology</topic><topic>Wastewater treatment</topic><topic>Wastewater treatment plants</topic><topic>Water Microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Maestre‐Carballa, Lucia</creatorcontrib><creatorcontrib>Lluesma Gomez, Monica</creatorcontrib><creatorcontrib>Angla Navarro, Andrea</creatorcontrib><creatorcontrib>Garcia‐Heredia, Inmaculada</creatorcontrib><creatorcontrib>Martinez‐Hernandez, Francisco</creatorcontrib><creatorcontrib>Martinez‐Garcia, Manuel</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Maestre‐Carballa, Lucia</au><au>Lluesma Gomez, Monica</au><au>Angla Navarro, Andrea</au><au>Garcia‐Heredia, Inmaculada</au><au>Martinez‐Hernandez, Francisco</au><au>Martinez‐Garcia, Manuel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Insights into the antibiotic resistance dissemination in a wastewater effluent microbiome: bacteria, viruses and vesicles matter</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2019-12</date><risdate>2019</risdate><volume>21</volume><issue>12</issue><spage>4582</spage><epage>4596</epage><pages>4582-4596</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Wastewater treatment plants effluents are considered as hotspots for the dispersion of antibiotic resistance genes (ARGs) into natural ecosystems. The bacterial resistome (ARG collection in a metagenome) analyses have provided clues on antibacterial resistance dynamics. However, viruses and vesicles are frequently ignored. Here, we addressed the bacterial, viral and vesicle resistomes from a representative wastewater effluent in natural conditions and amended with polymyxin, which is used as a last resort antibiotic. Metagenomics showed that the natural prokaryotic resistome was vast (9000 ARG hits/Gb metagenome) and diverse, while viral resistome was two orders of magnitude lower (50 ARG hits/Gb metagenome) suggesting that viruses rarely encoded ARGs. After polymyxin amendment, data showed no ARG enrichment – including to polymyxin – in the microbiome. Remarkably, microbiomes responded to polymyxin with a vast release of putative vesicles (threefold increase compared with the control), which might be used as 'traps' to decrease the antibiotic concentration. Intriguingly, although polymyxin resistance genes (PRGs) were rare in the microbiome (0.018% of total ARG found), in the viral and vesicle fractions, PRGs were more abundant (0.5%–0.8% of total ARG found). Our data suggest that vesicles could have a more active role in the context of transmission of antibiotic resistances.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>31342640</pmid><doi>10.1111/1462-2920.14758</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-5056-1525</orcidid></addata></record> |
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| ispartof | Environmental microbiology, 2019-12, Vol.21 (12), p.4582-4596 |
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| subjects | Anti-Bacterial Agents - pharmacology Antibiotic resistance Antibiotics Bacteria Bacteria - drug effects Bacteria - genetics Disease hot spots Disease resistance Drug resistance Drug Resistance, Microbial Effluents Extracellular Vesicles Genes Genes, Bacterial Metagenome Microbiomes Microbiota - drug effects Vesicles Viruses Viruses - genetics Waste Water - microbiology Wastewater treatment Wastewater treatment plants Water Microbiology |
| title | Insights into the antibiotic resistance dissemination in a wastewater effluent microbiome: bacteria, viruses and vesicles matter |
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