Bacterial Dimethylsulfoniopropionate Biosynthesis in the East China Sea

Ji Liu,Brett Wagner Mackenzie,Yanfen Zheng,Jingli Liu,Ana Bermejo Martínez,Hao Sun,Haohui Zhong,Andrew R J Curson,Yunhui Zhang,Jonathan D Todd,Delei Song,Beth T Williams,Xiao-Hua Zhang,Chuang Sun

doi:10.3390/microorganisms9030657

Abstract

Dimethylsulfoniopropionate (DMSP) is one of Earth’s most abundant organosulfur molecules. Recently, many marine heterotrophic bacteria were shown to produce DMSP, but few studies have combined culture-dependent and independent techniques to study their abundance, distribution, diversity and activity in seawater or sediment environments. Here we investigate bacterial DMSP production potential in East China Sea (ECS) samples. Total DMSP (DMSPt) concentration in ECS seawater was highest in surface waters (SW) where phytoplankton were most abundant, and it decreased with depth to near bottom waters. However, the percentage of DMSPt mainly apportioned to bacteria increased from the surface to the near bottom water. The highest DMSP concentration was detected in ECS oxic surface sediment (OSS) where phytoplankton were not abundant. Bacteria with the genetic potential to produce DMSP and relevant biosynthesis gene transcripts were prominent in all ECS seawater and sediment samples. Their abundance also increased with depth and was highest in the OSS samples. Microbial enrichments for DMSP-producing bacteria from sediment and seawater identified many novel taxonomic groups of DMSP-producing bacteria. Different profiles of DMSP-producing bacteria existed between seawater and sediment samples and there are still novel DMSP-producing bacterial groups to be discovered in these environments. This study shows that heterotrophic bacteria significantly contribute to the marine DMSP pool and that their contribution increases with water depth and is highest in seabed surface sediment where DMSP catabolic potential is lowest. Furthermore, distinct bacterial groups likely produce DMSP in seawater and sediment samples, and many novel producing taxa exist, especially in the sediment.

Highlights

Dimethylsulfoniopropionate (DMSP) is an abundant organic sulfur compound that acts as a signal molecule [1], marine nutrient [2], and the main precursor of the climateactive gas dimethyl sulfide (DMS) through the action of DMSP lyase enzymes in the marine environment [2,3]
We investigate bacterial DMSP synthesis in surface seawater (SW), near bottom seawater (NBW) and oxic surface sediment (OSS) samples collected from the East China
The potential importance of heterotrophic bacterial DMSP production in the East China Sea (ECS) was studied in SW and NBW samples collected from three different sites P03, ME3 and P11, including an OSS sample from P03 (Figure 1, Tables S1 and S2)

Summary

Introduction

Dimethylsulfoniopropionate (DMSP) is an abundant organic sulfur compound that acts as a signal molecule [1], marine nutrient [2], and the main precursor of the climateactive gas dimethyl sulfide (DMS) through the action of DMSP lyase enzymes in the marine environment [2,3]. Microorganisms 2021, 9, 657 nuclei [6,7], though this theory was challenged by Quinn and Bates [8]. Many marine bacteria import DMSP and can degrade it via DMSP cleavage or DMSP demethylation pathways [2,9]. Excess MeSH produced by demethylation pathway, if not assimilated, reacts to form dissolved nonvolatile compounds, e.g., DOM–metal–MeSH complexes, which affect trace metal availability and chemistry in seawater [10]. DMSP is one of the most significant carbon sources and a major sulfur source for marine microbial communities, perhaps influencing metal and DOM cycles in the oceans

Results

Discussion

Conclusion