Unexpected insights on marine sulfur cycling from unlikely terrestrial beginnings

Published in Microbiology
Unexpected insights on marine sulfur cycling from unlikely terrestrial beginnings
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This manuscript arose from a successful Chinese Scholarship Council (CSC) funded collaboration between Ocean University of China and the University of East Anglia. On this adventure,  we uncovered significant findings relevant to global sulfur cycling that were far above what we initially anticipated. Our primary aims were to investigate the transfer and utilisation of the abundant organosulfur compound dimethylsulfoniopropionate (DMSP) from salt marsh plants to heterotrophic bacteria that inhabit their rhizospheres. Such a study was important because DMSP can have roles in signalling pathways and protection against salinity, cold and oxidative stress in the organisms that produce it. More relevantly here, when released into the environment, DMSP is imported by diverse organisms and either utilised for its antistress properties or assimilated as a key source of carbon and sulfur. Many organisms, particularly bacteria, catabolise bacteria via a DMSP cleavage pathway that yields >350 million tonnes of the climate-active gas and signalling molecule dimethylsulfide (DMS). DMS, known as the smell of the seaside, is the major bio-source of sulfur transferred from marine environments to the atmosphere. DMS oxidation products in the atmosphere act as cloud condensation nuclei, potentially impacting climate, and transfer sulfur back to terrestrial systems through precipitation to complete the global sulfur cycle.

Our study initially focused on an unusual rhizobacterium Gynuella sunshinyii, isolated from the salt marsh plants Carex scabrifolia and Spartina alterniflora, previously known or shown here, respectively, to produce DMSP. G. sunshinyii is itself well known for its ability to produce secondary metabolites, such as antifungals1, which we proposed might be produced to benefit the plants in return for DMSP as an osmolyte and/or nutrient. However, this hypothesis went out of the window when we discovered that G. sunshinyii produced DMSP itself to levels far surpassing those in its C. scabrifolia plant host and those in the model DMSP-producing bacterium Labrenzia aggregata, from which we identified the first DMSP biosynthesis gene2. Thus, we excitedly turned our attention to identifying how (the key genes and enzymes involved) and why Gynuella produced DMSP, especially considering this Gammaproteobacterium lacked all known DMSP synthesis enzymes.

Using functional genomics, we excitedly uncovered a bi-domain and bifunctional DMSP synthesis enzyme “DsyGD” in G. sunshinyii that produced DMSP from the transamination pathway intermediate 4-methylthio-2-hydroxybutyrate (MTHB). The N-terminal DsyG domain S-methylated MTHB to form 4-dimethylsulfonio-2-hydroxybutyrate (DMSHB), which was subsequently decarboxylated by the C-terminal DsyD domain to yield DMSP. Unusually, DsyGD was not seen in any other organism at high amino acid identity, and the origin of this enzyme is currently puzzling. However, DsyGD or single domain DsyG MTHB S-methyltransferases, were found at ~50% amino acid identity in filamentous Oscillatoriales cyanobacteria, such as Zarconia navalis, not previously known to produce DMSP. Interestingly, Z. navalis, which only contained a single DsyG and no DsyD domain, produced far more DMSHB than DMSP, implying that DMSHB may take on the role/s of DMSP in some organisms and environments. DMSP/DMSHB production and the transcription of dsyGD/dsyG was enhanced by increased salinity in these DMSP producers, and heterologous expression of DsyGD conferred enhanced salinity tolerance to Escherichia coli, implying that DMSHB and DMSP likely act as osmolytes within these cyano/bacteria. Although these DMSP-producing enzymes and the organisms containing them are no doubt interesting, especially in terms of their enzyme mechanisms that warrants future investigation, neither are particularly common in marine environments.

The major and most exciting findings of this study arose from our bioinformatic probing of marine eukaryotic phytoplankton transcriptomes with DsyGD sequences. Although there was no obvious DsyG or DsyD domains encoded within these transcriptomes, candidate methyltransferases with < 38 % amino acid identity to DsyG were found in many high, low and previously unknown accumulators of DMSP. These proteins, termed DSYE (in capitals to denote the eukaryotic host), were phylogenetically distinct to DsyG and separated into five separate clades, with representatives from each clades all showing MTHB S-methyltransferase activity. These included Chloroarachniophyta (Clade A), abundant and diverse Chlorophyta (Clade B) and Pelagophyceae (Clade C), Haptophyta (Clade D) and diatoms (Clade E). Thus, DSYE is a robust indicator of DMSP synthesis ability in important phytoplankton and its identification significantly expanded our ability to predict eukaryotic DMSP producers. Furthermore, DSYE sequences from picoeukaryotic chlorophytes, such as Ostreococcus and Micromonas, and more prominently, from bloom-forming Pelagophyceae species, such as Pelagomonas calceolate (one of the most abundant eukaryotic species in Earth’s oceans3), were far more abundant than any other known bacterial or phytoplankton DMSP synthesis gene in the Earth’s surface oceans. This highlighted the potential importance of bloom-forming Pelagophyceae, not previously thought to be important DMSP producers, Chlorophyta and other DSYE-containing phytoplankton in the production of one of the Earth’s most abundant and important sulfur compounds, global sulfur cycling and, potentially, in the generation of climate-active gases.

Figure 1 (A) Sampling process of Carex scabrifolia and the roots of C. scabrifolia (B, C). (D) brown tide bloom and bloom-forming algae of Aureococcus anophagefferens (E) in Qinhuagndao, China in 2012.

Figure 1 (A) Sampling process of Carex scabrifolia and the roots of C. scabrifolia (B, C). (D) brown tide bloom and bloom-forming algae of Aureococcus anophagefferens (E) in Qinhuagndao, China in 2012, the picture was provided by Dr. Ren-Cheng Yu.

This blog was finished by Jinyan Wang, Xiao-Hua Zhang and Jonathan D. Todd

 References

  1. Mavrodi, O. V. et al. Rhizosphere microbial communities of Spartina alterniflora and Juncus roemerianus from restored and natural tidal marshes on Deer Island, Mississippi. Front. Microbiol. 9, 03049 (2018).
  2. Curson, A. R. J. et al. Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Microbiol. 2, 17009 (2017).
  3. Guerin, N. et al. Genomic adaptation of the picoeukaryote Pelagomonas calceolata to iron-poor oceans revealed by a chromosome-scale genome sequence. Biol. 5, 983 (2022).

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