Persisting antibiotic resistance gene pollution and its association with human sewage sources in tropical marine beach waters

TY - JOUR

T1 - Persisting antibiotic resistance gene pollution and its association with human sewage sources in tropical marine beach waters

AU - Makkaew, Prasert

AU - Kongprajug, Akechai

AU - Chyerochana, Natcha

AU - Sresung, Montakarn

AU - Precha, Nopadol

AU - Mongkolsuk, Skorn

AU - Sirikanchana, Kwanrawee

N1 - Funding Information: This study was financially supported by Walailak University (Grant No. WU-IRG-63-025) and Chulabhorn Research Institute (Grant No. 312/3057). Publisher Copyright: © 2021 Elsevier GmbH

PY - 2021/9

Y1 - 2021/9

N2 - Antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) are pollutants of worldwide concern that threaten human health and ecosystems. Anthropogenic activities and wastewater could be ARB and ARG pollution sources; however, research on ARG abundance and microbial source tracking (MST) of contamination in tropical marine waters is limited. This study examined spatiotemporal variations of six ARGs (blaNDM, blaTEM, blaVIM, mcr-1, sul1, and tetQ) against the widely used antibiotic groups and a class 1 integron-integrase gene (intI1) at two Thai tropical recreational beaches (n = 41). Correlations between ARGs and sewage-specific MST markers (i.e., crAssphage and human polyomaviruses [HPyVs]) and fecal indicator bacteria (i.e., total coliforms, fecal coliforms, and enterococci) were also investigated. BlaTEM, intI1, sul1, and tetQ were ubiquitous at both beaches (85.4–100% detection rate); intI1 was the most abundant (3–6 orders in log10 copies/100 mL), followed by blaTEM (2–4 orders), sul1 (2–3 orders), and tetQ (2–4 orders). BlaNDM was found in 7.3% (up to 4 orders), and no mcr-1 was detected. Interestingly, blaVIM was prevalent at one beach (2–5 orders; n = 17), but found in only one sample at the other (4 orders). Temporal, but not spatial, differences were noticed; blaTEM was at higher levels in the wet season. IntI1 correlated with sul1 and tetQ (Spearman's rho = 0.47–0.97), suggesting potential horizontal gene transfer. CrAssphage, but not HPyVs, correlated with intI1, sul1, and tetQ (Spearman's rho = 0.50–0.74). Higher numbers of ARGs tended to co-occur in samples with higher crAssphage concentrations, implying sewage contribution to the marine water, with a persisting ARG background. This study provides insight into the ARG pollution status of tropical coastal waters and suggests crAssphage as a proxy for ARG pollution, which could facilitate effective management policies to minimize ARG dissemination in marine environments.

AB - Antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) are pollutants of worldwide concern that threaten human health and ecosystems. Anthropogenic activities and wastewater could be ARB and ARG pollution sources; however, research on ARG abundance and microbial source tracking (MST) of contamination in tropical marine waters is limited. This study examined spatiotemporal variations of six ARGs (blaNDM, blaTEM, blaVIM, mcr-1, sul1, and tetQ) against the widely used antibiotic groups and a class 1 integron-integrase gene (intI1) at two Thai tropical recreational beaches (n = 41). Correlations between ARGs and sewage-specific MST markers (i.e., crAssphage and human polyomaviruses [HPyVs]) and fecal indicator bacteria (i.e., total coliforms, fecal coliforms, and enterococci) were also investigated. BlaTEM, intI1, sul1, and tetQ were ubiquitous at both beaches (85.4–100% detection rate); intI1 was the most abundant (3–6 orders in log10 copies/100 mL), followed by blaTEM (2–4 orders), sul1 (2–3 orders), and tetQ (2–4 orders). BlaNDM was found in 7.3% (up to 4 orders), and no mcr-1 was detected. Interestingly, blaVIM was prevalent at one beach (2–5 orders; n = 17), but found in only one sample at the other (4 orders). Temporal, but not spatial, differences were noticed; blaTEM was at higher levels in the wet season. IntI1 correlated with sul1 and tetQ (Spearman's rho = 0.47–0.97), suggesting potential horizontal gene transfer. CrAssphage, but not HPyVs, correlated with intI1, sul1, and tetQ (Spearman's rho = 0.50–0.74). Higher numbers of ARGs tended to co-occur in samples with higher crAssphage concentrations, implying sewage contribution to the marine water, with a persisting ARG background. This study provides insight into the ARG pollution status of tropical coastal waters and suggests crAssphage as a proxy for ARG pollution, which could facilitate effective management policies to minimize ARG dissemination in marine environments.

KW - Antibiotic resistance genes

KW - crAssphage

KW - Fecal pollution

KW - Microbial source tracking

KW - Quantitative PCR

KW - Seawater

KW - Southeast asia

UR - http://www.scopus.com/inward/record.url?scp=85116938195&partnerID=8YFLogxK

U2 - 10.1016/j.ijheh.2021.113859

DO - 10.1016/j.ijheh.2021.113859

M3 - Article

C2 - 34655856

AN - SCOPUS:85116938195

SN - 1438-4639

VL - 238

JO - INTERNATIONAL JOURNAL OF HYGIENE AND ENVIRONMENTAL HEALTH

JF - INTERNATIONAL JOURNAL OF HYGIENE AND ENVIRONMENTAL HEALTH

M1 - 113859

ER -