Biogeographic traits of dimethyl sulfide and dimethylsulfoniopropionate cycling in polar oceans

Abstract

Background Dimethyl sulfide (DMS) is the dominant volatile organic sulfur in global oceans. The predominant source of oceanic DMS is the cleavage of dimethylsulfoniopropionate (DMSP), which can be produced by marine bacteria and phytoplankton. Polar oceans, which represent about one fifth of Earth’s surface, contribute significantly to the global oceanic DMS sea-air flux. However, a global overview of DMS and DMSP cycling in polar oceans is still lacking and the key genes and the microbial assemblages involved in DMSP/DMS transformation remain to be fully unveiled. Results Here, we systematically investigated the biogeographic traits of 16 key microbial enzymes involved in DMS/DMSP cycling in 60 metagenomic samples from polar waters, together with 174 metagenome and 151 metatranscriptomes from non-polar Tara Ocean dataset. Our analyses suggest that intense DMS/DMSP cycling occurs in the polar oceans. DMSP demethylase (DmdA), DMSP lyases (DddD, DddP, and DddK), and trimethylamine monooxygenase (Tmm, which oxidizes DMS to dimethylsulfoxide) were the most prevalent bacterial genes involved in global DMS/DMSP cycling. Alphaproteobacteria (Pelagibacterales) and Gammaproteobacteria appear to play prominent roles in DMS/DMSP cycling in polar oceans. The phenomenon that multiple DMS/DMSP cycling genes co-occurred in the same bacterial genome was also observed in metagenome assembled genomes (MAGs) from polar oceans. The microbial assemblages from the polar oceans were significantly correlated with water depth rather than geographic distance, suggesting the differences of habitats between surface and deep waters rather than dispersal limitation are the key factors shaping microbial assemblages involved in DMS/DMSP cycling in polar oceans. Conclusions Overall, this study provides a global overview of the biogeographic traits of known bacterial genes involved in DMS/DMSP cycling from the Arctic and Antarctic oceans, laying a solid foundation for further studies of DMS/DMSP cycling in polar ocean microbiome at the enzymatic, metabolic, and processual levels.

The Microbiological Drivers of Temporally Dynamic Dimethylsulfoniopropionate Cycling Processes in Australian Coastal Shelf Waters

“…These genes have been identified in diverse lineages of bacteria, including members of the SAR116 and Roseobacter clade ( Todd et al, 2011 , 2012 ; Choi et al, 2015 ), and, most recently, with the discovery of dddK in the SAR11 clade ( Sun et al, 2021 ). Of these genes, dddK has been reported as the most dominant in pelagic open water environments ( Teng et al, 2021 ), while the most abundant in productive coastal waters is the Roseobacter and SAR116-associated dddP ( Nowinski et al, 2019a ).…”

“…DMS oxidation is performed by bacteria that possess one of three known enzymes, a multicomponent monooxygenase (DsoABCDEF), a DMS hydrogenase (DdhABC), and trimethylamine monooxygenase (Tmm) ( Horinouchi et al, 1999 ; McDevitt et al, 2002 ; Chen et al, 2011 ). The most abundant gene encoding bacterial DMS oxidation is tmm ( Teng et al, 2021 ), which requires methylamines to convert DMS to DMSO, is estimated to be found in 20% of all bacterial cells and is notably found in the SAR11 clade and Roseobacter group ( Chen et al, 2011 ; Lidbury et al, 2016 ).…”

“…Notably, there is often no clear linear relationship between DMSP and DMS concentrations, which has been attributed to differential DMS production among phytoplankton assemblages and bacterial degradation of DMSP ( Levasseur et al, 1996 ). The abundance of bacterial genes encoding enzymes that catalyze DMS(P) degradation (e.g., dmdA, tmm , and dddP ) exhibits wide geographical distributions and is detected in tropical to polar environments ( Teng et al, 2021 ). These genes have also been shown to significantly vary in abundance over time ( Nowinski et al, 2019a ), although their seasonal dynamics, relationships with environmental DMS(P) levels, and links to bacterial assemblage structure have not been examined in detail.…”

Recent insights into oceanic dimethylsulfoniopropionate biosynthesis and catabolism

“…Studies on the bacterial DMSP‐degrading genes such as dmdA and dddP have been carried out in varied marine environments (Cui et al ., 2015; Kuek et al ., 2016; Zeng et al ., 2016; Liu et al ., 2018; Nowinski et al ., 2019; Cui et al ., 2020; Teng et al ., 2021) and reported that these genes are taxonomically diverse and widespread across almost all major oceans, from tropical waters to the polar sea (Peng et al ., 2012; Cui et al ., 2015; Zeng et al ., 2016; Teng et al ., 2021). In comparison to DMSP catabolism, there were few molecular studies on environmental DMSP production and these showed bacterial DMSP production to be significant in surface coastal sediment, marine sediment and seawater, sea surface microlayer, estuary, and deep‐ocean environments (Williams et al ., 2019; Song et al ., 2020; Sun et al ., 2020; Zheng et al ., 2020; Sun et al ., 2021; Zhang et al ., 2021).…”

Correction to: Biogeographic traits of dimethyl sulfide and dimethylsulfoniopropionate cycling in polar oceans

“…Following the publication of the original article [ 1 ], the author reported that there is an error in one of the authors name. The name of the 8th co-author of this article should be “Guangfu Luo”, not “Guangfu Lu”.…”