Butenolide inhibits marine fouling by altering the primary metabolism of three target organisms

Yifan Zhang; Huoming Zhang; Lisheng He; Changdong Liu; Ying Xü; Pei-Yuan Qian

doi:10.1021/cb200545s

Butenolide inhibits marine fouling by altering the primary metabolism of three target organisms

Yifan Zhang, Huoming Zhang, Lisheng He, Changdong Liu, Ying Xü, Pei-Yuan Qian

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Abstract

Butenolide is a very promising antifouling compound that inhibits ship hull fouling by a variety of marine organisms, but its antifouling mechanism was previously unknown. Here we report the first study of butenolides molecular targets in three representative fouling organisms. In the barnacle Balanus (=Amphibalanus) amphitrite, butenolide bound to acetyl-CoA acetyltransferase 1 (ACAT1), which is involved in ketone body metabolism. Both the substrate and the product of ACAT1 increased larval settlement under butenolide treatment, suggesting its functional involvement. In the bryozoan Bugula neritina, butenolide bound to very long chain acyl-CoA dehydrogenase (ACADVL), actin, and glutathione S-transferases (GSTs). ACADVL is the first enzyme in the very long chain fatty acid β-oxidation pathway. The inhibition of this primary pathway for energy production in larvae by butenolide was supported by the finding that alternative energy sources (acetoacetate and pyruvate) increased larval attachment under butenolide treatment. In marine bacterium Vibrio sp. UST020129-010, butenolide bound to succinyl-CoA synthetase β subunit (SCSβ) and inhibited bacterial growth. ACAT1, ACADVL, and SCSβ are all involved in primary metabolism for energy production. These findings suggest that butenolide inhibits fouling by influencing the primary metabolism of target organisms. © 2012 American Chemical Society.

Original language	English (US)
Pages (from-to)	1049-1058
Number of pages	10
Journal	ACS Chemical Biology
Volume	7
Issue number	6
DOIs	https://doi.org/10.1021/cb200545s
State	Published - Apr 10 2012

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank Y. Zhang and J. Sun for their help in UPLC-MS/MS analysis; S. Dash for her help in Vibrio sp. UST020129-010 bioassays and cultures; Z. F. Chen and H. Wang for their help in RNA extraction, cDNA synthesis, and real-time PCR analysis; Y. H. Wong for his help in bugula sample collection; J. P. Ren, P. Chen, H. S. Wong, and R. Ko for their help in thiolase characterization; and S. Bougouffa, K. Matsumura, A. Wu, and J. R. Wu for their helpful comments on a draft of this manuscript. This study was supported by a grant from China Ocean Mineral Resources Research and Development (DY125-15-T-02), a joint research grant from the RGC of the HKSAR and the NSFC of China (N_HKUST602/09), and an award (SA-C0040/UK-C0016) from the King Abdullah University of Science and Technology to P. Y. Qian.

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Biochemistry
Molecular Medicine

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title = "Butenolide inhibits marine fouling by altering the primary metabolism of three target organisms",

abstract = "Butenolide is a very promising antifouling compound that inhibits ship hull fouling by a variety of marine organisms, but its antifouling mechanism was previously unknown. Here we report the first study of butenolides molecular targets in three representative fouling organisms. In the barnacle Balanus (=Amphibalanus) amphitrite, butenolide bound to acetyl-CoA acetyltransferase 1 (ACAT1), which is involved in ketone body metabolism. Both the substrate and the product of ACAT1 increased larval settlement under butenolide treatment, suggesting its functional involvement. In the bryozoan Bugula neritina, butenolide bound to very long chain acyl-CoA dehydrogenase (ACADVL), actin, and glutathione S-transferases (GSTs). ACADVL is the first enzyme in the very long chain fatty acid β-oxidation pathway. The inhibition of this primary pathway for energy production in larvae by butenolide was supported by the finding that alternative energy sources (acetoacetate and pyruvate) increased larval attachment under butenolide treatment. In marine bacterium Vibrio sp. UST020129-010, butenolide bound to succinyl-CoA synthetase β subunit (SCSβ) and inhibited bacterial growth. ACAT1, ACADVL, and SCSβ are all involved in primary metabolism for energy production. These findings suggest that butenolide inhibits fouling by influencing the primary metabolism of target organisms. {\textcopyright} 2012 American Chemical Society.",

author = "Yifan Zhang and Huoming Zhang and Lisheng He and Changdong Liu and Ying X{\"u} and Pei-Yuan Qian",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Y. Zhang and J. Sun for their help in UPLC-MS/MS analysis; S. Dash for her help in Vibrio sp. UST020129-010 bioassays and cultures; Z. F. Chen and H. Wang for their help in RNA extraction, cDNA synthesis, and real-time PCR analysis; Y. H. Wong for his help in bugula sample collection; J. P. Ren, P. Chen, H. S. Wong, and R. Ko for their help in thiolase characterization; and S. Bougouffa, K. Matsumura, A. Wu, and J. R. Wu for their helpful comments on a draft of this manuscript. This study was supported by a grant from China Ocean Mineral Resources Research and Development (DY125-15-T-02), a joint research grant from the RGC of the HKSAR and the NSFC of China (N_HKUST602/09), and an award (SA-C0040/UK-C0016) from the King Abdullah University of Science and Technology to P. Y. Qian.",

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doi = "10.1021/cb200545s",

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T1 - Butenolide inhibits marine fouling by altering the primary metabolism of three target organisms

AU - Zhang, Yifan

AU - Zhang, Huoming

AU - He, Lisheng

AU - Liu, Changdong

AU - Xü, Ying

AU - Qian, Pei-Yuan

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Y. Zhang and J. Sun for their help in UPLC-MS/MS analysis; S. Dash for her help in Vibrio sp. UST020129-010 bioassays and cultures; Z. F. Chen and H. Wang for their help in RNA extraction, cDNA synthesis, and real-time PCR analysis; Y. H. Wong for his help in bugula sample collection; J. P. Ren, P. Chen, H. S. Wong, and R. Ko for their help in thiolase characterization; and S. Bougouffa, K. Matsumura, A. Wu, and J. R. Wu for their helpful comments on a draft of this manuscript. This study was supported by a grant from China Ocean Mineral Resources Research and Development (DY125-15-T-02), a joint research grant from the RGC of the HKSAR and the NSFC of China (N_HKUST602/09), and an award (SA-C0040/UK-C0016) from the King Abdullah University of Science and Technology to P. Y. Qian.

PY - 2012/4/10

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N2 - Butenolide is a very promising antifouling compound that inhibits ship hull fouling by a variety of marine organisms, but its antifouling mechanism was previously unknown. Here we report the first study of butenolides molecular targets in three representative fouling organisms. In the barnacle Balanus (=Amphibalanus) amphitrite, butenolide bound to acetyl-CoA acetyltransferase 1 (ACAT1), which is involved in ketone body metabolism. Both the substrate and the product of ACAT1 increased larval settlement under butenolide treatment, suggesting its functional involvement. In the bryozoan Bugula neritina, butenolide bound to very long chain acyl-CoA dehydrogenase (ACADVL), actin, and glutathione S-transferases (GSTs). ACADVL is the first enzyme in the very long chain fatty acid β-oxidation pathway. The inhibition of this primary pathway for energy production in larvae by butenolide was supported by the finding that alternative energy sources (acetoacetate and pyruvate) increased larval attachment under butenolide treatment. In marine bacterium Vibrio sp. UST020129-010, butenolide bound to succinyl-CoA synthetase β subunit (SCSβ) and inhibited bacterial growth. ACAT1, ACADVL, and SCSβ are all involved in primary metabolism for energy production. These findings suggest that butenolide inhibits fouling by influencing the primary metabolism of target organisms. © 2012 American Chemical Society.

AB - Butenolide is a very promising antifouling compound that inhibits ship hull fouling by a variety of marine organisms, but its antifouling mechanism was previously unknown. Here we report the first study of butenolides molecular targets in three representative fouling organisms. In the barnacle Balanus (=Amphibalanus) amphitrite, butenolide bound to acetyl-CoA acetyltransferase 1 (ACAT1), which is involved in ketone body metabolism. Both the substrate and the product of ACAT1 increased larval settlement under butenolide treatment, suggesting its functional involvement. In the bryozoan Bugula neritina, butenolide bound to very long chain acyl-CoA dehydrogenase (ACADVL), actin, and glutathione S-transferases (GSTs). ACADVL is the first enzyme in the very long chain fatty acid β-oxidation pathway. The inhibition of this primary pathway for energy production in larvae by butenolide was supported by the finding that alternative energy sources (acetoacetate and pyruvate) increased larval attachment under butenolide treatment. In marine bacterium Vibrio sp. UST020129-010, butenolide bound to succinyl-CoA synthetase β subunit (SCSβ) and inhibited bacterial growth. ACAT1, ACADVL, and SCSβ are all involved in primary metabolism for energy production. These findings suggest that butenolide inhibits fouling by influencing the primary metabolism of target organisms. © 2012 American Chemical Society.

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JF - ACS Chemical Biology

IS - 6

ER -

Butenolide inhibits marine fouling by altering the primary metabolism of three target organisms

Abstract

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