Utilization of diverse organophosphorus pollutants by marine bacteria

Dragana Despotovic*, Einav Aharon, Olena Trofimyuk, Artem Dubovetskyi, Kesava Phaneendra Cherukuri, Yacov Ashani, Or Eliason, Martin Sperfeld, Haim Leader, Andrea Castelli, Laura Fumagalli, Alon Savidor, Yishai Levin, Liam Longo*, Einat Segev*, Dan Tawfik

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

10 Citations (Scopus)

Abstract

Anthropogenic organophosphorus compounds (AOPCs), such as phosphotriesters, are used extensively as plasticizers, flame retardants, nerve agents, and pesticides. To date, only a handful of soil bacteria bearing a phosphotriesterase (PTE), the key enzyme in the AOPC degradation pathway, have been identified. Therefore, the extent to which bacteria are capable of utilizing AOPCs as a phosphorus source, and how widespread this adaptation may be, remains unclear. Marine environments with phosphorus limitation and increasing levels of pollution by AOPCs may drive the emergence of PTE activity. Here, we report the utilization of diverse AOPCs by four model marine bacteria and 17 bacterial isolates from the Mediterranean Sea and the Red Sea. To unravel the details of AOPC utilization, two PTEs from marine bacteria were isolated and characterized, with one of the enzymes belonging to a protein family that, to our knowledge, has never before been associated with PTE activity. When expressed in Escherichia coli with a phosphodiesterase, a PTE isolated from a marine bacterium enabled growth on a pesticide analog as the sole phosphorus source. Utilization of AOPCs may provide bacteria a source of phosphorus in depleted environments and offers a prospect for the bioremediation of a pervasive class of anthropogenic pollutants.

Original languageEnglish
Article numbere2203604119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number32
DOIs
Publication statusPublished - 9 Aug 2022

Funding

ACKNOWLEDGMENTS. We are grateful to Prof. Miguel Frada (The Hebrew University of Jerusalem) and Prof. Yael Kiro (Weizmann Institute of Science) for collecting water samples from the Red Sea and the Mediterranean Sea; Dr. Michael Etzerodt (Aarhus University) for sharing the isatin hydrolase gene; and Prof. Jonathan Todd (University of East Anglia) and Prof. Andrew Johnston (University of East Anglia) for kindly providing the Ruegeria strains. We acknowledge Roni Beiralas and Yemima Duchin Rapp for their assistance in establishing protocols for marine bacteria cultivation. We thank Dr. Shifra Ben-Dor for valuable discussions. We acknowledge insightful comments on the manuscript from Prof. Maria Vila-Costa, Prof. Ita Gruic-Sovulj, and Prof. Danica Galonić-Fujimori. D.D. and D.S.T. were supported by the Defense Threat Reduction Agency of the US Department of Defense (HDTRA1-17-0057). E.S. was funded by the Israeli Science Foundation (ISF 947/18), the Peter and Patricia Gruber Foundation, the Minerva Foundation with funding from the Federal German Ministry for Education and Research, the Angel Faivovich Foundation for Ecological Research, the Estate of Emile Mimran, and The Maurice and Vivienne Wohl Biology Endowment.

All Science Journal Classification (ASJC) codes

  • General

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