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Article: Antibiotic resistance genes and human bacterial pathogens: Co-occurrence, removal, and enrichment in municipal sewage sludge digesters

TitleAntibiotic resistance genes and human bacterial pathogens: Co-occurrence, removal, and enrichment in municipal sewage sludge digesters
Authors
KeywordsAntibiotic resistance genes
Human bacterial pathogens
Metagenomics
Network analysis
Sewage sludge
Issue Date2016
PublisherPergamon. The Journal's web site is located at http://www.elsevier.com/locate/watres
Citation
Water Research, 2016, v. 91, p. 1-10 How to Cite?
AbstractUnderstanding which/how antibiotic resistance genes (ARGs) contribute to increased acquisition of resistance by pathogens in aquatic environments are challenges of profound significance. We explored the co-occurrence and removal versus enrichment of ARGs and human bacterial pathogens (HBPs) in municipal sewage sludge digesters. We combined metagenomic detection of a wide spectrum of 323 ARGs and 83 HBPs with a correlation-based statistical approach and charted a network of their co-occurrence relationships. The results indicate that most ARGs and a minor proportion of HBPs (mainly Collinsella aerofaciens, Streptococcus salivarius and Gordonia bronchialis) could not be removed by anaerobic digestion, revealing a biological risk of post-digestion sludge in disseminating antibiotic resistance and pathogenicity. Moreover, preferential co-occurrence patterns were evident within one ARG type (e.g., multidrug, beta-lactam, and aminoglycoside) and between two different ARG types (i.e., aminoglycoside and beta-lactam), possibly implicating co-effects of antibiotic selection pressure and co-resistance on shaping antibiotic resistome in sewage sludge. Unlike beta-lactam resistance genes, ARGs of multidrug and macrolide-lincosamide-streptogramin tended to co-occur more with HBPs. Strikingly, we presented evidence that the most straightforward biological origin of an ARG-species co-occurring event is a hosting relationship. Furthermore, a significant and robust HBP-species co-occurrence correlation provides a proper scenario for nominating HBP indicators (e.g., Bifidobacterium spp. are perfect indicators of C. aerofaciens; r = 0.92–0.99 and P-values < 0.01). Combined, this study demonstrates a creative and effective network-based metagenomic approach for exploring ARG hosts and HBP indicators and assessing ARGs acquisition by HBPs in human-impacted environments where ARGs and HBPs may co-thrive.
Persistent Identifierhttp://hdl.handle.net/10722/293316
ISSN
2023 Impact Factor: 11.4
2023 SCImago Journal Rankings: 3.596
ISI Accession Number ID

 

DC FieldValueLanguage
dc.contributor.authorJu, F-
dc.contributor.authorLi, B-
dc.contributor.authorMa, L-
dc.contributor.authorWang, Y-
dc.contributor.authorHuang, D-
dc.contributor.authorZhang, T-
dc.date.accessioned2020-11-23T08:14:59Z-
dc.date.available2020-11-23T08:14:59Z-
dc.date.issued2016-
dc.identifier.citationWater Research, 2016, v. 91, p. 1-10-
dc.identifier.issn0043-1354-
dc.identifier.urihttp://hdl.handle.net/10722/293316-
dc.description.abstractUnderstanding which/how antibiotic resistance genes (ARGs) contribute to increased acquisition of resistance by pathogens in aquatic environments are challenges of profound significance. We explored the co-occurrence and removal versus enrichment of ARGs and human bacterial pathogens (HBPs) in municipal sewage sludge digesters. We combined metagenomic detection of a wide spectrum of 323 ARGs and 83 HBPs with a correlation-based statistical approach and charted a network of their co-occurrence relationships. The results indicate that most ARGs and a minor proportion of HBPs (mainly Collinsella aerofaciens, Streptococcus salivarius and Gordonia bronchialis) could not be removed by anaerobic digestion, revealing a biological risk of post-digestion sludge in disseminating antibiotic resistance and pathogenicity. Moreover, preferential co-occurrence patterns were evident within one ARG type (e.g., multidrug, beta-lactam, and aminoglycoside) and between two different ARG types (i.e., aminoglycoside and beta-lactam), possibly implicating co-effects of antibiotic selection pressure and co-resistance on shaping antibiotic resistome in sewage sludge. Unlike beta-lactam resistance genes, ARGs of multidrug and macrolide-lincosamide-streptogramin tended to co-occur more with HBPs. Strikingly, we presented evidence that the most straightforward biological origin of an ARG-species co-occurring event is a hosting relationship. Furthermore, a significant and robust HBP-species co-occurrence correlation provides a proper scenario for nominating HBP indicators (e.g., Bifidobacterium spp. are perfect indicators of C. aerofaciens; r = 0.92–0.99 and P-values < 0.01). Combined, this study demonstrates a creative and effective network-based metagenomic approach for exploring ARG hosts and HBP indicators and assessing ARGs acquisition by HBPs in human-impacted environments where ARGs and HBPs may co-thrive.-
dc.languageeng-
dc.publisherPergamon. The Journal's web site is located at http://www.elsevier.com/locate/watres-
dc.relation.ispartofWater Research-
dc.subjectAntibiotic resistance genes-
dc.subjectHuman bacterial pathogens-
dc.subjectMetagenomics-
dc.subjectNetwork analysis-
dc.subjectSewage sludge-
dc.titleAntibiotic resistance genes and human bacterial pathogens: Co-occurrence, removal, and enrichment in municipal sewage sludge digesters-
dc.typeArticle-
dc.identifier.emailZhang, T: zhangt@hkucc.hku.hk-
dc.identifier.authorityZhang, T=rp00211-
dc.description.naturelink_to_subscribed_fulltext-
dc.identifier.doi10.1016/j.watres.2015.11.071-
dc.identifier.pmid26773390-
dc.identifier.scopuseid_2-s2.0-84953263285-
dc.identifier.hkuros319460-
dc.identifier.volume91-
dc.identifier.spage1-
dc.identifier.epage10-
dc.identifier.isiWOS:000371189100001-
dc.publisher.placeUnited Kingdom-
dc.identifier.issnl0043-1354-

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