Abstract

ABSTRACTQuorum sensing (QS) is a widespread process in bacteria used to coordinate gene expression with cell density, diffusion dynamics, and spatial distribution through the production of diffusible chemical signals. To date, most studies on QS have focused on model bacteria that are amenable to genetic manipulation and capable of high growth rates, but many environmentally important bacteria have been overlooked. For example, representatives of proteobacteria that participate in nitrification, the aerobic oxidation of ammonia to nitrate via nitrite, produce QS signals called acyl-homoserine lactones (AHLs). Nitrification emits nitrogen oxide gases (NO, NO2, and N2O), which are potentially hazardous compounds that contribute to global warming. Despite considerable interest in nitrification, the purpose of QS in the physiology/ecology of nitrifying bacteria is poorly understood. Through a quorum quenching approach, we investigated the role of QS in a well-studied AHL-producing nitrite oxidizer, Nitrobacter winogradskyi. We added a recombinant AiiA lactonase to N. winogradskyi cultures to degrade AHLs to prevent their accumulation and to induce a QS-negative phenotype and then used mRNA sequencing (mRNA-Seq) to identify putative QS-controlled genes. Our transcriptome analysis showed that expression of nirK and nirK cluster genes (ncgABC) increased up to 19.9-fold under QS-proficient conditions (minus active lactonase). These data led to us to query if QS influenced nitrogen oxide gas fluxes in N. winogradskyi. Production and consumption of NOx increased and production of N2O decreased under QS-proficient conditions. Quorum quenching transcriptome approaches have broad potential to identify QS-controlled genes and phenotypes in organisms that are not genetically tractable.

Highlights

  • Quorum sensing (QS) is a widespread process in bacteria used to coordinate gene expression with cell density, diffusion dynamics, and spatial distribution through the production of diffusible chemical signals

  • NH3 is oxidized to NO2Ϫ by ammonia oxidizers, including bacteria (AOB) and archaea (AOA), while NO2Ϫ is oxidized to NO3Ϫ by nitriteoxidizing bacteria (NOB)

  • Nitrification is a key part of the nitrogen cycle in natural, agricultural, and industrial systems and is a contributor to gas emissions of nitric oxide (NO), nitrogen oxides (NOx), and nitrous oxide (N2O), which are hazardous gases that contribute to global warming [11, 17]

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Summary

Introduction

Quorum sensing (QS) is a widespread process in bacteria used to coordinate gene expression with cell density, diffusion dynamics, and spatial distribution through the production of diffusible chemical signals. Our transcriptome analysis showed that expression of nirK and nirK cluster genes (ncgABC) increased up to 19.9-fold under QS-proficient conditions (minus active lactonase) These data led to us to query if QS influenced nitrogen oxide gas fluxes in N. winogradskyi. Quorum sensing (QS) is a widespread process that bacteria use to coordinate gene expression with cell density, diffusion dynamics, and spatial distribution through the production of diffusible chemical signals [1, 2]. Many welldesigned studies have introduced null mutations in the QS signal synthase and/or signal receptor-transcriptional regulator genes to determine what genes and phenotypes are controlled by QS [1] While this approach has significantly increased our understanding, many other QS-proficient organisms that are not genetically tractable have not been thoroughly studied. The luxI and luxR genes are commonly located adjacent to each other in the genome and are generally positively autoregulated [1]

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