Abstract
The volatile microbial metabolite 2-methylisoborneol (2-MIB) is a root cause of taste and odor issues in freshwater. Although current evidence suggests that 2-MIB is not toxic, this compound degrades water quality and presents problems for water treatment. To address these issues, cyanobacteria and actinomycetes, the major producers of 2-MIB, have been investigated extensively. In this study, two 2-MIB producing strains, coded as Pseudanabaena sp. and Planktothricoids raciborskii, were used in order to elucidate the genetic background, light regulation, and biochemical mechanisms of 2-MIB biosynthesis in cyanobacteria. Genome walking and PCR methods revealed that two adjacent genes, SAM-dependent methyltransferanse gene and monoterpene cyclase gene, are responsible for GPP methylation and subsequent cyclization to 2-MIB in cyanobacteria. These two genes are located in between two homologous cyclic nucleotide-binding protein genes that may be members of the Crp-Fnr regulator family. Together, this sequence of genes forms a putative operon. The synthesis of 2-MIB is similar in cyanobacteria and actinomycetes. Comparison of the gene arrangement and functional sites between cyanobacteria and other organisms revealed that gene recombination and gene transfer probably occurred during the evolution of 2-MIB-associated genes. All the microorganisms examined have a common origin of 2-MIB biosynthesis capacity, but cyanobacteria represent a unique evolutionary lineage. Gene expression analysis suggested that light is a crucial, but not the only, active regulatory factor for the transcription of 2-MIB synthesis genes. This light-regulated process is immediate and transient. This study is the first to identify the genetic background and evolution of 2-MIB biosynthesis in cyanobacteria, thus enhancing current knowledge on 2-MIB contamination of freshwater.
Highlights
Microorganisms are an important source of terpenoid metabolites, including monoterpenes, sesquiterpenes, and diterpenes, in natural environments
Using Headspace solid phase micro-extraction (HS-SPME) coupled with GCMS, the main odorous components produced by Pseudanabaena sp. dqh15 and Planktothricoides raciborskii CHAB 3331 were isolated and determined
Cyanobacteria are a frequent source of these problems due to the production of 2-MIB and geosmin [15,17,19]
Summary
Microorganisms are an important source of terpenoid metabolites, including monoterpenes, sesquiterpenes, and diterpenes, in natural environments. Among the numerous terpenoid compounds, geosmin and 2-methylisoborneol (2-MIB) belonging to the sesquiterpenes and monoterpenes, respectively, and are widely known for their odorous and volatile properties. These two terpenoid alcohols are synthesized and usually secreted as secondary metabolites by microorganisms, such as fungi, myxobacteria, actinmycetes, and cyanobacteria [1,2,3,4,5]. Geosmin was isolated and identified as a degraded sesquiterpenoid alcohol [1], while 2-MIB was first isolated in actinomycetes as a methylated monoterpene [6]. Low concentrations of 2-MIB (less than 10 ng/L) could cause detectable odorous problems in drinking waters and usually leads to rejection by consumers [8]
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