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

Yunhui Zhang,Shun Zhou,Ji Liu,Xiao-Hua Zhang,Yanfen Zheng,Min Yu,Delei Song,Haohui Zhong,Jonathan D Todd

doi:10.3389/fmicb.2020.00157

Abstract

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.

Highlights

Eight billion tons of the organosulfur compound dimethylsulfoniopropionate (DMSP) is produced in Earth’s surface oceans (Galí et al, 2015)
Our study shows that: DMSP concentrations were far higher in marine sediment than those in surface waters per unit volume; DMSP-producing bacteria with DsyB were present in most seawater and sediment samples; bacteria with the genetic potential to cleave DMSP generating DMS were far more abundant than those with dmdA in all tested sediment, but that dmdA was more prominent in surface waters; bacteria with mddA were very abundant in marine sediment but not in seawater; DMSP catabolic potential via known pathways was rare in OTSP samples, yet genes for DMS, DMSO, and MeSH cycling pathways were more abundant
Such studies are focused on bacteria since the vast majority of known genes involved in the cycling of DMSP and related compounds were discovered in bacteria and are predominantly bacterial, with a few exceptions notably Alma1, detected DMSP catabolic gene (dddP) and DSYB, and TpMT2 (Curson et al, 2011a, 2017, 2008; Johnston, 2015; Zhang et al, 2019), which occur in eukaryotes

Summary

Introduction

Eight billion tons of the organosulfur compound dimethylsulfoniopropionate (DMSP) is produced in Earth’s surface oceans (Galí et al, 2015). The key methylthiohydroxybutyrate S-methyltransferase enzyme of the Met transamination pathway is catalyzed by three distinct S-adenosyl-Met (SAM)-dependent S-methyltransferase enzymes in different organisms These are DsyB in some alphaproteobacteria (Curson et al, 2017), DSYB in algae and corals (Curson et al, 2018), and TpMMT in the diatom Thalassiosira pseudonana (Kageyama et al, 2018). Williams et al predicted that ∼104 and 108 bacteria per mL/g of surface seawater or sediment have the genetic potential to produce DMSP. Curson et al (2018) found that there were ∼two-fold more algal DSYB transcripts than those for the bacterial dsyB gene in North Pacific Ocean coastal seawater samples This supports algae as the major DMSP producers in photic seawater

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Conclusion