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Applied and Environmental Microbiology, March 2005, p. 1291-1299, Vol. 71, No. 3
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.3.1291-1299.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Rapid Acyl-Homoserine Lactone Quorum Signal Biodegradation in Diverse Soils{dagger}

Ya-Juan Wang and Jared Renton Leadbetter*

Environmental Science and Engineering, W. M. Keck Laboratories, California Institute of Technology, Pasadena, California

Received 17 August 2004/ Accepted 8 October 2004

Signal degradation impacts all communications. Although acyl-homoserine lactone (acyl-HSL) quorum-sensing signals are known to be degraded by defined laboratory cultures, little is known about their stability in nature. Here, we show that acyl-HSLs are biodegraded in soils sampled from diverse U.S. sites and by termite hindgut contents. When amended to samples at physiologically relevant concentrations, 14C-labeled acyl-HSLs were mineralized to 14CO2 rapidly and, at most sites examined, without lag. A lag-free turf soil activity was characterized in further detail. Heating or irradiation of the soil prior to the addition of radiolabel abolished mineralization, whereas protein synthesis inhibitors did not. Mineralization exhibited an apparent Km of 1.5 µM acyl-HSL, ca. 1,000-fold lower than that reported for a purified acyl-HSL lactonase. Under optimal conditions, acyl-HSL degradation proceeded at a rate of 13.4 nmol · h–1 · g of fresh weight soil–1. Bioassays established that the final extent of signal inactivation was greater than for its full conversion to CO2 but that the two processes were well coupled kinetically. A most probable number of 4.6 x 105 cells · g of turf soil–1 degraded physiologically relevant amounts of hexanoyl-[1-14C]HSL to 14CO2. It would take chemical lactonolysis months to match the level of signal decay achieved in days by the observed biological activity. Rapid decay might serve either to quiet signal cross talk that might otherwise occur between spatially separated microbial aggregates or as a full system reset. Depending on the context, biological signal decay might either promote or complicate cellular communications and the accuracy of population density-based controls on gene expression in species-rich ecosystems.

* Corresponding author. Mailing address: Mailcode 138-78, California Institute of Technology, Pasadena, CA 91125. Phone: (626) 395-4182. Fax: (626) 395-2940. E-mail: jleadbetter{at}caltech.edu.

{dagger} This paper is dedicated to John A. Breznak in celebration of his 60th birthday and his 30 years as a research leader.

Applied and Environmental Microbiology, March 2005, p. 1291-1299, Vol. 71, No. 3
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.3.1291-1299.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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