A novel pathway producing dimethylsulphide in bacteria is widespread in soil environments

Carrión, Ornella; Curson, Andrew R. J.; Kumaresan, Deepak; Fu, Yu-Song; Lang, Andrew S.; Mercadé, Montse; Todd, Jonathan D.

doi:10.1038/ncomms7579

Cited by 92 publications

(87 citation statements)

References 52 publications

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“…DMSP is metabolized in P. aeruginosa PAO1 through the demethylation pathway (19), which generates acetaldehyde, carbon dioxide, and methanethiol as products. Methanethiol can be converted into hydrogen sulfide via methanethiol oxidase, or it can be methylated by a thiol methyltransferase to yield DMS (2,20,21). There is no experimental or bioinformatic evidence supporting the existence of a methanethiol oxidase in P. aeruginosa PAO1, and although a methanethiol-specific methyltransferase has been characterized (20), there are no proteins similar to this enzyme encoded in the genome of P. aeruginosa PAO1.…”

Section: Discussionmentioning

confidence: 99%

SfnR2 Regulates Dimethyl Sulfide-Related Utilization in Pseudomonas aeruginosa PAO1

et al. 2019

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Dimethyl sulfide (DMS) is a volatile sulfur compound produced mainly from the degradation of dimethylsulfoniopropionate (DMSP) in marine environments. DMS undergoes oxidation to form dimethyl sulfoxide (DMSO), dimethyl sulfone (DMSO 2 ), and methanesulfonate (MSA), all of which occur in terrestrial environments and are accessible for consumption by various microorganisms. The purpose of the present study was to determine how the enhancer-binding proteins SfnR1 and SfnR2 contribute to the utilization of DMS and its derivatives in Pseudomonas aeruginosa PAO1. First, results from cell growth experiments showed that deletion of either sfnR2 or sfnG, a gene encoding a DMSO 2 -monooxygenase, significantly inhibits the ability of P. aeruginosa PAO1 to use DMSP, DMS, DMSO, and DMSO 2 as sulfur sources. Deletion of the sfnR1 or msuEDC genes, which encode a MSA desulfurization pathway, did not abolish the growth of P. aeruginosa PAO1 on any sulfur compound tested. Second, data collected from ␤-galactosidase assays revealed that the msuEDC-sfnR1 operon and the sfnG gene are induced in response to sulfur limitation or nonpreferred sulfur sources, such as DMSP, DMS, and DMSO, etc. Importantly, SfnR2 (and not SfnR1) is essential for this induction. Expression of sfnR2 is induced under sulfur limitation but independently of SfnR1 or SfnR2. Finally, the results of this study suggest that the main function of SfnR2 is to direct the initial activation of the msuEDC-sfnR1 operon in response to sulfur limitation or nonpreferred sulfur sources. Once expressed, SfnR1 contributes to the expression of msuEDC-sfnR1, sfnG, and other target genes involved in DMS-related metabolism in P. aeruginosa PAO1. IMPORTANCE Dimethyl sulfide (DMS) is an important environmental source of sulfur, carbon, and/or energy for microorganisms. For various bacteria, including Pseudomonas, Xanthomonas, and Azotobacter, DMS utilization is thought to be controlled by the transcriptional regulator SfnR. Adding more complexity, some bacteria, such as Acinetobacter baumannii, Enterobacter cloacae, and Pseudomonas aeruginosa, possess two, nonidentical SfnR proteins. In this study, we demonstrate that SfnR2 and not SfnR1 is the principal regulator of DMS metabolism in P. aeruginosa PAO1. Results suggest that SfnR1 has a supportive but nonessential role in the positive regulation of genes required for DMS utilization. This study not only enhances our understanding of SfnR regulation but, importantly, also provides a framework for addressing gene regulation through dual SfnR proteins in other bacteria.

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Section: Discussionmentioning

confidence: 99%

SfnR2 Regulates Dimethyl Sulfide-Related Utilization in Pseudomonas aeruginosa PAO1

et al. 2019

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“…In contrast, MddA was identified in Pseudomonas deceptionensis (Carrión et al, 2015(Carrión et al, , 2017, but many diverse aerobic and anaerobic bacteria and cyanobacteria also contain MddA and likely methylate MeSH to generate DMS (Drotar et al, 1987;Kiene and Hines, 1995;Stets et al, 2004;Carrión et al, 2015). The mddA gene is present in varied environmental metagenomes, but thus far has been found to be much more abundant in terrestrial than in marine environments (Carrión et al, 2015(Carrión et al, , 2017(Carrión et al, , 2019. For example, 5-76% of bacteria in soil metagenomes were predicted to contain mddA, compared to 9.6% of bacteria from surface saltmarsh sediment samples and ≤ 0.5% of bacteria in seawater metagenomes.…”

Section: Introductionmentioning

confidence: 89%

“…Metagenomics analysis suggested that the mtoX gene was widely distributed in seawater (0.4-45.6% of bacteria), freshwater (5.3% of bacteria), soil environments (∼6.3% of bacteria; Eyice et al, 2018), and saltmarsh sediment (4.0%; Carrión et al, 2019). In contrast, MddA was identified in Pseudomonas deceptionensis (Carrión et al, 2015(Carrión et al, , 2017, but many diverse aerobic and anaerobic bacteria and cyanobacteria also contain MddA and likely methylate MeSH to generate DMS (Drotar et al, 1987;Kiene and Hines, 1995;Stets et al, 2004;Carrión et al, 2015). The mddA gene is present in varied environmental metagenomes, but thus far has been found to be much more abundant in terrestrial than in marine environments (Carrión et al, 2015(Carrión et al, , 2017(Carrión et al, , 2019.…”

Section: Introductionmentioning

confidence: 99%

Metagenomic Insights Into the Cycling of Dimethylsulfoniopropionate and Related Molecules in the Eastern China Marginal Seas

et al. 2020

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The microbial cycling of dimethylsulfoniopropionate (DMSP) and its gaseous catabolites dimethylsulfide (DMS) and methanethiol (MeSH) are important processes in the global sulfur cycle, marine microbial food webs, signaling pathways, atmospheric chemistry, and potentially climate regulation. Many functional genes have been identified and used to study the genetic potential of microbes to produce and catabolize these organosulfur compounds in different marine environments. Here, we sampled seawater, marine sediment and hydrothermal sediment, and polymetallic sulfide in the eastern Chinese marginal seas and analyzed their microbial communities for the genetic potential to cycle DMSP, DMS, and MeSH using metagenomics. DMSP was abundant in all sediment samples, but was fivefold less prominent in those from hydrothermal samples. Indeed, Yellow Sea (YS) sediment samples had DMSP concentrations two orders of magnitude higher than in surface water samples. Bacterial genetic potential to synthesize DMSP (mainly in Rhodobacteraceae bacteria) was far higher than for phytoplankton in all samples, but particularly in the sediment where no algal DMSP synthesis genes were detected. Thus, we propose bacteria as important DMSP producers in these marine sediments. DMSP catabolic pathways mediated by the DMSP lyase DddP (prominent in Pseudomonas and Mesorhizobium bacteria) and DMSP demethylase DmdA enzymes (prominent in Rhodobacteraceae bacteria) and MddA-mediated MeSH S-methylation were very abundant in Bohai Sea and Yellow Sea sediments (BYSS) samples. In contrast, the genetic potential for DMSP degradation was very low in the hydrothermal sediment samples-dddP was the only catabolic gene detected and in only one sample. However, the potential for DMS production from MeSH (mddA) and DMS oxidation (dmoA and ddhA) was relatively abundant. This metagenomics study does not provide conclusive evidence for DMSP cycling; however, it does highlight the potential importance of bacteria in the synthesis and catabolism of DMSP and related compounds in diverse sediment environments.

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“…Unraveling the microbial composition and processes occurring in these systems will not only help optimize the technical processes but can also lead to the discovery of novel pathways and organisms. In the era of next-generation sequencing techniques, metagenomics-based approaches have enabled the discovery of a suite of novel microbial pathways (Schleper et al, 2005;Bryant et al, 2007;Ettwig et al, 2010;Carrión et al, 2015) and the expansion of the tree of life (Brown et al, 2015). Some of these discoveries have been made in technical systems; for example, novel candidate phyla and expanded metabolic versatility have been identified in aerobic and anaerobic bioreactors (Wexler et al, 2005;Rinke et al, 2013;Nobu et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology ofNitrospiraspp.

et al. 2016

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Rapid gravity sand filtration is a drinking water production technology widely used around the world. Microbially catalyzed processes dominate the oxidative transformation of ammonia, reduced manganese and iron, methane and hydrogen sulfide, which may all be present at millimolar concentrations when groundwater is the source water. In this study, six metagenomes from various locations within a groundwater-fed rapid sand filter (RSF) were analyzed. The community gene catalog contained most genes of the nitrogen cycle, with particular abundance in genes of the nitrification pathway. Genes involved in different carbon fixation pathways were also abundant, with the reverse tricarboxylic acid cycle pathway most abundant, consistent with an observed Nitrospira dominance. From the metagenomic data set, 14 near-complete genomes were reconstructed and functionally characterized. On the basis of their genetic content, a metabolic and geochemical model was proposed. The organisms represented by draft genomes had the capability to oxidize ammonium, nitrite, hydrogen sulfide, methane, potentially iron and manganese as well as to assimilate organic compounds. A composite Nitrospira genome was recovered, and amo-containing Nitrospira genome contigs were identified. This finding, together with the high Nitrospira abundance, and the abundance of atypical amo and hao genes, suggests the potential for complete ammonium oxidation by Nitrospira, and a major role of Nitrospira in the investigated RSFs and potentially other nitrifying environments.

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A novel pathway producing dimethylsulphide in bacteria is widespread in soil environments

Cited by 92 publications

References 52 publications

SfnR2 Regulates Dimethyl Sulfide-Related Utilization in Pseudomonas aeruginosa PAO1

SfnR2 Regulates Dimethyl Sulfide-Related Utilization in Pseudomonas aeruginosa PAO1

Metagenomic Insights Into the Cycling of Dimethylsulfoniopropionate and Related Molecules in the Eastern China Marginal Seas

Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology ofNitrospiraspp.

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