TY - JOUR
T1 - DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton
AU - Curson, Andrew R.J.
AU - Williams, Beth T.
AU - Pinchbeck, Benjamin J.
AU - Sims, Leanne P.
AU - Martínez, Ana Bermejo
AU - Rivera, Peter Paolo L.
AU - Kumaresan, Deepak
AU - Mercadé, Elena
AU - Spurgin, Lewis G.
AU - Carrión, Ornella
AU - Moxon, Simon
AU - Cattolico, Rose Ann
AU - Kuzhiumparambil, Unnikrishnan
AU - Guagliardo, Paul
AU - Clode, Peta L.
AU - Raina, Jean Baptiste
AU - Todd, Jonathan D.
N1 - P Rivera was not affiliated to SAMS at the time of publication.
Funding Information:
Funding from the Natural Environment Research Council (NE/J01138X/1, NE/ M004449/1, NE/N002385/1 and NE/P012671/1) supported work in J.D.T.’s laboratory. B.T.W. was supported by an NERC EnvEast grant (NE/L002582/1) and A.B.M. was supported by a BBSRC Norwich Research Park Biosciences Doctoral Training Partnership grant (BB/M011216/1). The NanoSIMS work was supported by an Australian Research Council Grant (DE160100636) to J.-B.R. We thank P. Wells and M. Giardina for general technical support, T. Mock for supplying Fragilariopsis cylindrus, and R. Green, J. Liu and C. Murrell for advice and discussion of results. We also acknowledge the Tara Oceans Consortium for providing metagenomic sequence data, and the facilities at the Australian Microscopy & Microanalysis Research Facility at the Centre for Microscopy, Characterisation & Analysis, University of Western Australia, a facility funded by the University, State and Commonwealth Governments.
Publisher Copyright:
© 2018 The Author(s).
Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.
PY - 2018/4/1
Y1 - 2018/4/1
N2 - Dimethylsulfoniopropionate (DMSP) is a globally important organosulfur molecule and the major precursor for dimethyl sulfide. These compounds are important info-chemicals, key nutrients for marine microorganisms, and are involved in global sulfur cycling, atmospheric chemistry and cloud formation1-3. DMSP production was thought to be confined to eukaryotes, but heterotrophic bacteria can also produce DMSP through the pathway used by most phytoplankton4, and the DsyB enzyme catalysing the key step of this pathway in bacteria was recently identified5. However, eukaryotic phytoplankton probably produce most of Earth's DMSP, yet no DMSP biosynthesis genes have been identified in any such organisms. Here we identify functional dsyB homologues, termed DSYB, in many phytoplankton and corals. DSYB is a methylthiohydroxybutryate methyltransferase enzyme localized in the chloroplasts and mitochondria of the haptophyte Prymnesium parvum, and stable isotope tracking experiments support these organelles as sites of DMSP synthesis. DSYB transcription levels increased with DMSP concentrations in different phytoplankton and were indicative of intracellular DMSP. Identification of the eukaryotic DSYB sequences, along with bacterial dsyB, provides the first molecular tools to predict the relative contributions of eukaryotes and prokaryotes to global DMSP production. Furthermore, evolutionary analysis suggests that eukaryotic DSYB originated in bacteria and was passed to eukaryotes early in their evolution.
AB - Dimethylsulfoniopropionate (DMSP) is a globally important organosulfur molecule and the major precursor for dimethyl sulfide. These compounds are important info-chemicals, key nutrients for marine microorganisms, and are involved in global sulfur cycling, atmospheric chemistry and cloud formation1-3. DMSP production was thought to be confined to eukaryotes, but heterotrophic bacteria can also produce DMSP through the pathway used by most phytoplankton4, and the DsyB enzyme catalysing the key step of this pathway in bacteria was recently identified5. However, eukaryotic phytoplankton probably produce most of Earth's DMSP, yet no DMSP biosynthesis genes have been identified in any such organisms. Here we identify functional dsyB homologues, termed DSYB, in many phytoplankton and corals. DSYB is a methylthiohydroxybutryate methyltransferase enzyme localized in the chloroplasts and mitochondria of the haptophyte Prymnesium parvum, and stable isotope tracking experiments support these organelles as sites of DMSP synthesis. DSYB transcription levels increased with DMSP concentrations in different phytoplankton and were indicative of intracellular DMSP. Identification of the eukaryotic DSYB sequences, along with bacterial dsyB, provides the first molecular tools to predict the relative contributions of eukaryotes and prokaryotes to global DMSP production. Furthermore, evolutionary analysis suggests that eukaryotic DSYB originated in bacteria and was passed to eukaryotes early in their evolution.
UR - http://www.scopus.com/inward/record.url?scp=85042531789&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85042531789&partnerID=8YFLogxK
U2 - 10.1038/s41564-018-0119-5
DO - 10.1038/s41564-018-0119-5
M3 - Article
C2 - 29483657
AN - SCOPUS:85042531789
SN - 2058-5276
VL - 3
SP - 430
EP - 439
JO - Nature Microbiology
JF - Nature Microbiology
IS - 4
ER -