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Rapid Acyl-Homoserine Lactone Quorum Signal Biodegradation in Diverse Soils

Wang, Ya-Juan and Leadbetter, Jared Renton (2005) Rapid Acyl-Homoserine Lactone Quorum Signal Biodegradation in Diverse Soils. Applied and Environmental Microbiology, 71 (3). pp. 1291-1299. ISSN 0099-2240. PMCID PMC1065188. doi:10.1128/AEM.71.3.1291-1299.2005.

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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.

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Leadbetter, Jared Renton0000-0002-7033-0844
Additional Information:© 2005, American Society for Microbiology. Received 17 August 2004/ Accepted 8 October 2004 This research was supported by grants from the USDA (CSREES 2001-01242) and by a generous gift from William Davidow and family. The Long-Term Ecological Research Program at Michigan State University's Kellogg Biological Station is supported by the NSF and the Michigan Agricultural Experiment Station. We thank D. Newman for liquid scintillation counter usage; L. Thomashow for providing agricultural soil samples from Pullman, Wash.; A. Corbin for providing KBS-LTER soil samples; and J. Hering, A. Kappler, E. R. Leadbetter, J. Suflita, our laboratory colleagues, and several anonymous reviewers of this and prior work for their insightful comments and suggestions. This paper is dedicated to John A. Breznak in celebration of his 60th birthday and his 30 years as a research leader.
Funding AgencyGrant Number
Department of AgricultureCSREES 2001-01242
William Davidow and familyUNSPECIFIED
Michigan Agricultural Experiment StationUNSPECIFIED
Issue or Number:3
PubMed Central ID:PMC1065188
Record Number:CaltechAUTHORS:WANaem05
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:1851
Deposited By: Archive Administrator
Deposited On:20 Feb 2006
Last Modified:08 Nov 2021 19:43

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