TY - JOUR
T1 - Integrated multi-omics investigations reveal the key role of synergistic microbial networks in removing plasticizer di-(2-ethylhexyl) phthalate from estuarine sediments
AU - Ting-Shyang Wei, Sean
AU - Chen, Yi Lung
AU - Wu, Yu Wei
AU - Wu, Tien Yu
AU - Lai, Yi Li
AU - Wang, Po Hsiang
AU - Ismail, Wael
AU - Lee, Tzong Huei
AU - Chiang, Yin Ru
N1 - Funding Information:
This study was supported by the Ministry of Science and Technology of Taiwan (MOST 109-2221-E-001-002 and 110-2222-E-008-002) and Academia Sinica Career Development Award (AS-CDA-110-L13). Yi-Lung Chen is supported by Research Grants for New Teachers of College of Science, Soochow University, Taiwan. Po-Hsiang Wang is supported by the Research and Development Office and Research Center for Sustainable Environmental Technology, National Central University, Taiwan.
Funding Information:
We thank the High Throughput Genomics Core Facility hosted by the Biodiversity Research Center at Academia Sinica for conducting the next-generation sequencing experiments. This core facility is funded by the Academia Sinica Core Facility and Innovative Instrument Project (AS-CFII-108-114). We also thank Yu-Ching Wu for performing UPLC-HRMS at the Small Molecule Metabolomics Core Facility, Institute of Plant and Microbial Biology. We have no conflicts of interest to declare.
Publisher Copyright:
© 2021 American Society for Microbiology. All rights reserved.
PY - 2021/6
Y1 - 2021/6
N2 - Di-(2-ethylhexyl) phthalate (DEHP) is the most widely used plasticizer worldwide, with an annual global production of more than 8 million tons. Because of its improper disposal, endocrine-disrupting DEHP often accumulates in estuarine sediments in industrialized countries at submillimolar levels, resulting in adverse effects on both ecosystems and human beings. The microbial degraders and biodegradation pathways of DEHP in O2-limited estuarine sediments remain elusive. Here, we employed an integrated meta-omics approach to identify the DEHP degradation pathway and major degraders in this ecosystem. Estuarine sediments were treated with DEHP or its derived metabolites, o-phthalic acid and benzoic acid. The rate of DEHP degradation in denitrifying mesocosms was two times slower than that of o-phthalic acid, suggesting that side chain hydrolysis of DEHP is the rate-limiting step of anaerobic DEHP degradation. On the basis of microbial community structures, functional gene expression, and metabolite profile analysis, we proposed that DEHP biodegradation in estuarine sediments is mainly achieved through synergistic networks between denitrifying proteobacteria. Acidovorax and Sedimenticola are the major degraders of DEHP side chains; the resulting o-phthalic acid is mainly degraded by Aestuariibacter through the UbiD-dependent benzoyl coenzyme A (benzoyl-CoA) pathway. We isolated and characterized Acidovorax sp. strain 210- 6 and its extracellular hydrolase, which hydrolyzes both alkyl side chains of DEHP. Interestingly, genes encoding DEHP/mono-(2-ethylhexyl) phthalate (MEHP) hydrolase and phthaloyl-CoA decarboxylase-key enzymes for side chain hydrolysis and o-phthalic acid degradation, respectively-are flanked by transposases in these proteobacterial genomes, indicating that DEHP degradation capacity is likely transferred horizontally in microbial communities.
AB - Di-(2-ethylhexyl) phthalate (DEHP) is the most widely used plasticizer worldwide, with an annual global production of more than 8 million tons. Because of its improper disposal, endocrine-disrupting DEHP often accumulates in estuarine sediments in industrialized countries at submillimolar levels, resulting in adverse effects on both ecosystems and human beings. The microbial degraders and biodegradation pathways of DEHP in O2-limited estuarine sediments remain elusive. Here, we employed an integrated meta-omics approach to identify the DEHP degradation pathway and major degraders in this ecosystem. Estuarine sediments were treated with DEHP or its derived metabolites, o-phthalic acid and benzoic acid. The rate of DEHP degradation in denitrifying mesocosms was two times slower than that of o-phthalic acid, suggesting that side chain hydrolysis of DEHP is the rate-limiting step of anaerobic DEHP degradation. On the basis of microbial community structures, functional gene expression, and metabolite profile analysis, we proposed that DEHP biodegradation in estuarine sediments is mainly achieved through synergistic networks between denitrifying proteobacteria. Acidovorax and Sedimenticola are the major degraders of DEHP side chains; the resulting o-phthalic acid is mainly degraded by Aestuariibacter through the UbiD-dependent benzoyl coenzyme A (benzoyl-CoA) pathway. We isolated and characterized Acidovorax sp. strain 210- 6 and its extracellular hydrolase, which hydrolyzes both alkyl side chains of DEHP. Interestingly, genes encoding DEHP/mono-(2-ethylhexyl) phthalate (MEHP) hydrolase and phthaloyl-CoA decarboxylase-key enzymes for side chain hydrolysis and o-phthalic acid degradation, respectively-are flanked by transposases in these proteobacterial genomes, indicating that DEHP degradation capacity is likely transferred horizontally in microbial communities.
KW - Acidovorax
KW - Anaerobic catabolic pathways
KW - Denitrifying bacteria
KW - Di-(2-ethylhexyl) phthalate
KW - Endocrine disruptor
KW - Metagenomics
KW - Phthalate esters
UR - http://www.scopus.com/inward/record.url?scp=85107407300&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85107407300&partnerID=8YFLogxK
U2 - 10.1128/mSystems.00358-21
DO - 10.1128/mSystems.00358-21
M3 - Article
AN - SCOPUS:85107407300
SN - 2379-5077
VL - 6
JO - mSystems
JF - mSystems
IS - 3
M1 - e00358-21
ER -