Bacteria are important dimethylsulfoniopropionate producers in marine aphotic and high-pressure environments

Zheng, Yanfen; Wang, Jinyan; Zhou, Shun; Zhang, Yunhui; Liu, Ji; Xue, Chun-Xu; Williams, Beth T.; Zhao, Xiuxiu; Zhao, Li; Zhu, Xiaoyu; Sun, Chuang; Zhang, Honghai; Xiao, Tian; Yang, Gui‐Peng; Todd, Jonathan D.; Zhang, Xiao‐Hua

doi:10.1038/s41467-020-18434-4

Cited by 87 publications

(79 citation statements)

References 58 publications

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“…Despite these information, little is known about the microbial eukaryotic communities and metabolic potentials in the deeper seawaters (8,727–11,000 m) of the Mariana Trench, where unique microbial populations (e.g., increased amount of SAR406, hydrocarbon-degrading microbes) have been observed ( Ichino et al, 2015 ; Nunoura et al, 2015 ; Liu et al, 2018 , 2019b ; Gao et al, 2019 ). In addition, whether microbial eukaryotes exhibit unique high-pressure adaptation mechanisms as found in bacteria and archaea in our previous studies ( Zheng et al, 2020 ; Zhong et al, 2020 ) is still unknown. Thus, knowledge of microbial eukaryotes at the bottom of the Mariana Trench, the deepest ocean part on Earth, is necessary for a better understanding of their ecological roles and potential adaptability.…”

Section: Introductionmentioning

confidence: 88%

Shift and Metabolic Potentials of Microbial Eukaryotic Communities Across the Full Depths of the Mariana Trench

et al. 2021

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Microbial eukaryotes are widespread and play important roles in marine ecosystems. However, their ecological characteristics in the deep sea (>1,000 m), especially hadal trenches, were largely unknown. Here, we investigated the diversity and metabolic potentials of microbial eukaryotes along the whole water column of the Mariana Trench by metagenomics. Our results showed clear depth-related distribution of microbial eukaryotic community and associated metabolic potentials. Surface seawater was dominated by phototrophic/mixotrophic groups (e.g., Dinoflagellata) and genes involved in biosynthesis (photosynthesis and fatty acid biosynthesis), while deep (bathypelagic and/or hadal) seawaters were enriched with heterotrophic groups (e.g., Bicoecea) and genes related to digestion (lysosomal enzymes and V-type ATPase) and carbohydrate metabolism. Co-occurrence analysis revealed high intra-domain connectivity, indicating that microbial eukaryotic composition was more influenced by microbial eukaryotes themselves than bacteria. Increased abundance of genes associated with unsaturated fatty acid biosynthesis likely plays a role in resisting high hydrostatic pressure. Top1 and hupB genes, responsible for the formation and stabilization of DNA structure, were unique and abundant in the hadal zone and thus may be helpful to stabilize DNA structure in the deep sea. Overall, our results provide insights into the distribution and potential adaptability of microbial eukaryotes in the hadal zone.

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Section: Introductionmentioning

confidence: 88%

Shift and Metabolic Potentials of Microbial Eukaryotic Communities Across the Full Depths of the Mariana Trench

et al. 2021

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“…The organosulfur molecule dimethylsulfoniopropionate (DMSP) is produced in massive amounts by many marine phytoplankton, macroalgae, angiosperms, bacteria, and animals ( Curson et al, 2018 ; Stefels, 2000 ; Otte et al, 2004 ; Curson et al, 2017 ; Raina et al, 2013 ). DMSP can function as an antioxidant, osmoprotectant, predator deterrent, cryoprotectant, protectant against hydrostatic pressure, chemoattractant and may enhance the production of quorum-sensing molecules ( Sunda et al, 2002 ; Cosquer et al, 1999 ; Wolfe et al, 1997 ; Karsten et al, 1996 ; Zheng et al, 2020 ; Seymour et al, 2010 ; Johnson et al, 2016 ). DMSP also has important roles in global sulfur and nutrient cycling ( Kiene et al, 2000 ; Charlson et al, 1987 ).…”

Section: Introductionmentioning

confidence: 99%

A novel ATP dependent dimethylsulfoniopropionate lyase in bacteria that releases dimethyl sulfide and acryloyl-CoA

Wang

Chen

et al. 2021

eLife

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Dimethylsulfoniopropionate (DMSP) is an abundant and ubiquitous organosulfur molecule in marine environments with important roles in global sulfur and nutrient cycling. Diverse DMSP lyases in some algae, bacteria and fungi cleave DMSP to yield gaseous dimethyl sulfide (DMS), an infochemical with important roles in atmospheric chemistry. Here we identified a novel ATP-dependent DMSP lyase, DddX. DddX belongs to the acyl-CoA synthetase superfamily and is distinct from the eight other known DMSP lyases. DddX catalyses the conversion of DMSP to DMS via a two-step reaction: the ligation of DMSP with CoA to form the intermediate DMSP-CoA, which is then cleaved to DMS and acryloyl-CoA. The novel catalytic mechanism was elucidated by structural and biochemical analyses. DddX is found in several Alphaproteobacteria, Gammaproteobacteria and Firmicutes, suggesting that this new DMSP lyase may play an overlooked role in DMSP/DMS cycles.

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“…The abundance of dsyB was normalized by the 16S rRNA gene copies obtained in our previous study (Zhang et al, 2021), and the proportion of DMSP-producing bacteria in SCS sediment samples (containing dsyB only since mmtN cannot be detected) were predicted by qPCR. DsyB was predicted to be in 0.0007-0.0195% bacteria (Supplementary Table 2), which is far lower than previously reported predictions (0.02-3.6%) in marine sediment samples (Williams et al, 2019;Zheng et al, 2020). Note that normalization conducted in this way is not overly accurate due to the multiple copies of the 16S rRNA gene in some bacteria.…”

Section: Quantification Of Dimethylsulfoniopropionate Biosynthesis and Catabolic Genesmentioning

confidence: 63%

Dimethylsulfoniopropionate Biosynthetic Bacteria in the Subseafloor Sediments of the South China Sea

Zhang

Sun

et al. 2021

Front. Microbiol.

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Dimethylsulfoniopropionate (DMSP) is one of Earth’s most abundant organosulfur molecules, and bacteria in marine sediments have been considered significant producers. However, the vertical profiles of DMSP content and DMSP-producing bacteria in subseafloor sediment have not been described. Here, we used culture-dependent and -independent methods to investigate microbial DMSP production and cycling potential in South China Sea (SCS) sediment. The DMSP content of SCS sediment decreased from 11.25 to 20.90 nmol g–1 in the surface to 0.56–2.08 nmol g–1 in the bottom layers of 8-m-deep subseafloor sediment cores (n = 10). Very few eukaryotic plastid sequences were detected in the sediment, supporting bacteria and not algae as important sediment DMSP producers. Known bacterial DMSP biosynthesis genes (dsyB and mmtN) were only predicted to be in 0.0007–0.0195% of sediment bacteria, but novel DMSP-producing isolates with potentially unknown DMSP synthesis genes and/or pathways were identified in these sediments, including Marinobacter (Gammaproteobacteria) and Erythrobacter (Alphaproteobacteria) sp. The abundance of bacteria with the potential to produce DMSP decreased with sediment depth and was extremely low at 690 cm. Furthermore, distinct DMSP-producing bacterial groups existed in surface and subseafloor sediment samples, and their abundance increased when samples were incubated under conditions known to enrich for DMSP-producing bacteria. Bacterial DMSP catabolic genes were also most abundant in the surface oxic sediments with high DMSP concentrations. This study extends the current knowledge of bacterial DMSP biosynthesis in marine sediments and implies that DMSP biosynthesis is not only confined to the surface oxic sediment zones. It highlights the importance of future work to uncover the DMSP biosynthesis genes/pathways in novel DMSP-producing bacteria.

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Bacteria are important dimethylsulfoniopropionate producers in marine aphotic and high-pressure environments

Cited by 87 publications

References 58 publications

Shift and Metabolic Potentials of Microbial Eukaryotic Communities Across the Full Depths of the Mariana Trench

Shift and Metabolic Potentials of Microbial Eukaryotic Communities Across the Full Depths of the Mariana Trench

A novel ATP dependent dimethylsulfoniopropionate lyase in bacteria that releases dimethyl sulfide and acryloyl-CoA

Dimethylsulfoniopropionate Biosynthetic Bacteria in the Subseafloor Sediments of the South China Sea

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