Transcriptomic analysis of the response of Acropora millepora to hypo-osmotic stress provides insights into DMSP biosynthesis by corals
Catalina AguilarJean‐Baptiste RainaCherie A. MottiSylvain ForêtDavid C. HaywardBruno LapeyreDavid G. BourneDavid J. Miller
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Dimethylsulfoniopropionate (DMSP) is a small sulphur compound which is produced in prodigious amounts in the oceans and plays a pivotal role in the marine sulfur cycle. Until recently, DMSP was believed to be synthesized exclusively by photosynthetic organisms; however we now know that corals and specific bacteria can also produce this compound. Corals are major sources of DMSP, but the molecular basis for its biosynthesis is unknown in these organisms.Here we used salinity stress, which is known to trigger DMSP production in other organisms, in conjunction with transcriptomics to identify coral genes likely to be involved in DMSP biosynthesis. We focused specifically on both adults and juveniles of the coral Acropora millepora: after 24 h of exposure to hyposaline conditions, DMSP concentrations increased significantly by 2.6 fold in adult corals and 1.2 fold in juveniles. Concomitantly, candidate genes enabling each of the necessary steps leading to DMSP production were up-regulated.The data presented strongly suggest that corals use an algal-like pathway to generate DMSP from methionine, and are able to rapidly change expression of the corresponding genes in response to environmental stress. However, our data also indicate that DMSP is unlikely to function primarily as an osmolyte in corals, instead potentially serving as a scavenger of ROS and as a molecular sink for excess methionine produced as a consequence of proteolysis and osmolyte catabolism in corals under hypo-osmotic conditions.Keywords:
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dimethylsulfide (数据管理系统) 和 dimethylsulfoniopropionate (DMSP ) 的时间的分布在 4 月和 2010 年 9 月期间在南部的黄海(SYS ) 被学习。数据管理系统的吝啬的集中(范围)，溶解并且在春天的表面水里的微粒 DMSP ( DMSPd 和 DMSPp )是 1.69 ( 0.484.92 )， 3.18 ( 0.686.75 )并且 15.81 ( 2.8252.33 ) nmol/L ，分别地并且在秋天的那些是 2.80 ( 1.335.10 )， 5.45 ( 2.1911.30 )并且 30.63 ( 6.24137.87 ) nmol/L 。总体上，在春天的数据管理系统和 DMSP 的分布与在秋天的那些完全不同。在 SYS 的中央部分，在春天的数据管理系统和 DMSP 的集中显然比在秋天的那些高，但是相反的状况在 34 的南方上被发现吗？？
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Dimethylsulfoniopropionate (DMSP), a key component of the global geochemical sulfur cycle, is a secondary metabolite produced in large quantities by marine phytoplankton and utilized as an osmoprotectant, thermoprotectant and antioxidant. Marine bacteria can use two pathways to degrade and catabolize DMSP, a demethylation pathway and a cleavage pathway that produces the climate active gas dimethylsulfide (DMS). Whether marine bacteria can also accumulate DMSP as an osmoprotectant to maintain the turgor pressure of the cell in response to changes in external osmolarity has received little attention. The marine halophile Vibrio parahaemolyticus, contains at least six osmolyte transporters, four betaine carnitine choline transport (BCCT) carriers BccT1-BccT4 and two ABC-family ProU transporters. In this study, we showed that DMSP is used as an osmoprotectant by V. parahaemolyticus and several other Vibrio species including V. cholerae and V. vulnificus Using a V. parahaemolyticus proU double mutant, we demonstrated that these ABC transporters are not required for DMSP uptake. However, a bccT null mutant lacking all four BCCTs had a growth defect compared to wild type in high salinity media supplemented with DMSP. Using mutants possessing only one functional BCCT in growth pattern assays, we identified two BCCT-family transporters, BccT1 and BccT2, which are carriers of DMSP. The only V. parahaemolyticus BccT homolog that V. cholerae and V. vulnificus possess is BccT3 and functional complementation in Escherichia coli MKH13 showed V. cholerae VcBccT3 could transport DMSP. In V. vulnificus strains, we identified and characterized an additional BCCT family transporter, which we named BccT5 that was also a carrier for DMSP.Importance DMSP is present in the marine environment, produced in large quantities by marine phytoplankton as an osmoprotectant, and is an important component of the global geochemical sulfur cycle. This algal osmolyte has not been previously investigated for its role in marine heterotrophic bacterial osmotic stress response. Vibrionaceae are marine species, many of which are halophiles exemplified by V. parahaemolyticus, a species that possesses at least six transporters for the uptake of osmolytes. Here, we demonstrated that V. parahaemolyticus and other Vibrio species can accumulate DMSP as an osmoprotectant and show that several BCCT family transporters uptake DMSP. These studies suggest that DMSP is a significant bacterial osmoprotectant, which may be important for understanding the fate of DMSP in the environment. DMSP is produced and present in coral mucus and Vibrio species form part of the microbial communities associated with them. The function of DMSP in these interactions is unclear, but could be an important driver for these associations allowing Vibrio proliferation. This work suggests that DMSP likely has an important role in heterotrophic bacteria ecology than previously appreciated.
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AME Aquatic Microbial Ecology Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsSpecials AME 76:133-147 (2015) - DOI: https://doi.org/10.3354/ame01772 Osmoprotective role of dimethylsulfoniopropionate (DMSP) for estuarine bacterioplankton Jessie Motard-Côté1,2,*, Ronald P. Kiene1,2 1Department of Marine Sciences, University of South Alabama, Mobile, Alabama 36688, USA 2Dauphin Island Sea Lab, 101 Bienville Blvd, Dauphin Island, Alabama 36528, USA *Corresponding author: jmotard-cote@disl.org ABSTRACT: Dimethylsulfoniopropionate (DMSP) is synthesized and used by marine phytoplankton as an osmolyte. Previous studies have shown that some of the dissolved DMSP (DMSPd) in seawater is taken up by bacterioplankton and not degraded. We tested the hypothesis that retention of DMSP provides some benefits to marine bacteria. In experiments with coastal seawater filtrates containing mainly bacteria, acute osmotic stresses of +5 and +10 ppt NaCl significantly inhibited bacterial production (BP) over 6 h, while the availability of 20 nM DMSPd relieved most of the BP inhibition. Partial relief of salt-induced inhibition of BP was observed with DMSPd concentrations as low as 2.5 nM, and DMSP was more effective at relieving osmotic stress than other compounds tested. Osmotic stresses resulted in a faster and greater overall uptake of DMSPd and accumulation of untransformed DMSP in bacterial cells (DMSPcell). Retained DMSP reached osmotically-significant intracellular concentrations of 54 mM in salt-stressed bacterial populations. Retention of DMSP was accompanied by a lower production of methanethiol (MeSH), suggesting a down-regulation of the demethylation/demethiolation pathway under osmotic stress. These results show that estuarine bacterioplankton can use DMSP as an osmoprotectant, retaining up to 54% of the available dissolved DMSP untransformed in their cells. This benefit provided by DMSP may help explain why some DMSP is retained in bacteria in the ocean, even under unchanging salinity. This retention slows down the cycling of DMSP, with potential implications for the trophic transfer of DMSP and its contributions to sulfur and carbon fluxes in the ocean. KEY WORDS: Osmolyte · Compatible solute · Salinity stress · Salt inhibition · Osmolarity · Sulfur cycle · DMSP retention · DMSP function Full text in pdf format PreviousNextCite this article as: Motard-Côté J, Kiene RP (2015) Osmoprotective role of dimethylsulfoniopropionate (DMSP) for estuarine bacterioplankton. Aquat Microb Ecol 76:133-147. https://doi.org/10.3354/ame01772 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in AME Vol. 76, No. 2. Online publication date: October 22, 2015 Print ISSN: 0948-3055; Online ISSN: 1616-1564 Copyright © 2015 Inter-Research.
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Mixed osmolytes: The degree to which one osmolyte affects the protein stabilizing ability of another
Mixtures of organic osmolytes occur in cells of many organisms, raising the question of whether their actions on protein stability are independent or synergistic. To investigate this question it is desirable to develop a system that permits evaluation of the effect of one osmolyte on the efficacy of another to either force-fold or denature a protein. A means of evaluating the efficacy of an osmolyte is provided by its m-value, an experimental quantity that measures the ability of the osmolyte to force a protein to unfold or fold. An experimental system is presented that enables evaluations of the m-values of osmolytes in the presence and absence of a second osmolyte. The experimental system involves use of a marginally stable protein in 10 mM buffer (pH 7, 200 mM salt, and 34 degrees C) that is at the midpoint of its native to denatured transition. These conditions enable determination of m-values for protecting and denaturing osmolytes in the presence and absence of a second osmolyte, permitting assessment of the extent to which the two osmolytes affect each other's efficacy. The two osmolytes investigated in this work are the denaturing osmolyte, urea, and the protecting osmolyte, sarcosine. Results show unequivocally that neither osmolyte alters the efficacy of the other in forcing the protein to fold or unfold-the osmolytes act independently on the protein despite their combined concentrations being in the multi-molar range. These osmolytes avoid altering one another's efficacy at these high concentrations because the number of osmolyte interaction sites on the protein is large and the binding constants are quite small. Consequently, the site occupancies are low enough in number that the two osmolytes neither compete nor cooperate in interacting with the protein.
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ABSTRACT Osmolyte accumulation and release can protect cells from abiotic stresses. In Escherichia coli , known mechanisms mediate osmotic stress-induced accumulation of K + glutamate, trehalose, or zwitterions like glycine betaine. Previous observations suggested that additional osmolyte accumulation mechanisms (OAMs) exist and their impacts may be abiotic stress specific. Derivatives of the uropathogenic strain CFT073 and the laboratory strain MG1655 lacking known OAMs were created. CFT073 grew without osmoprotectants in minimal medium with up to 0.9 M NaCl. CFT073 and its OAM-deficient derivative grew equally well in high- and low-osmolality urine pools. Urine-grown bacteria did not accumulate large amounts of known or novel osmolytes. Thus, CFT073 showed unusual osmotolerance and did not require osmolyte accumulation to grow in urine. Yeast extract and brain heart infusion stimulated growth of the OAM-deficient MG1655 derivative at high salinity. Neither known nor putative osmoprotectants did so. Glutamate and glutamine accumulated after growth with either organic mixture, and no novel osmolytes were detected. MG1655 derivatives retaining individual OAMs were created. Their abilities to mediate osmoprotection were compared at 15°C, 37°C without or with urea, and 42°C. Stress protection was not OAM specific, and variations in osmoprotectant effectiveness were similar under all conditions. Glycine betaine and dimethylsulfoniopropionate (DMSP) were the most effective. Trimethylamine- N -oxide (TMAO) was a weak osmoprotectant and a particularly effective urea protectant. The effectiveness of glycine betaine, TMAO, and proline as osmoprotectants correlated with their preferential exclusion from protein surfaces, not with their propensity to prevent protein denaturation. Thus, their effectiveness as stress protectants correlated with their ability to rehydrate the cytoplasm.
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The production and consumption of organic matter by marine organisms plays a central role in the marine carbon cycle. Labile organic compounds (metabolites) are the major currency of energetic demands and organismal interaction, but these compounds remain elusive because of their rapid turnover and concomitant minuscule concentrations in the dissolved organic matter pool. Organic osmolytes are a group of small metabolites synthesized at high intracellular concentrations (mM) to regulate cellular osmolarity and have the potential to be released as abundant dissolved substrates. Osmolytes may represent an essential currency of exchange among heterotrophic prokaryotes and primary and secondary producers in marine food webs. For example, the well-known metabolite dimethylsulfoniopropionate (DMSP) is used as an osmolyte by some phytoplankton and can be subsequently metabolized by 60% of the marine bacterial community, supplying up to 13% of the bacterial carbon demand and 100% of the bacterial sulfur demand. While marine osmolytes have been studied for decades, our understanding of their cycling and significance within microbial communities is still far from comprehensive. Here, we surveyed the genes responsible for synthesis, breakdown, and transport of 14 key osmolytes. We systematically searched for these genes across marine bacterial genomes ( n = 897) and protistan transcriptomes ( n = 652) using homologous protein profiles to investigate the potential for osmolyte metabolisms. Using the pattern of gene presence and absence, we infer the metabolic potential of surveyed microbes to interact with each osmolyte. Specifically, we identify: (1) complete pathways for osmolyte synthesis in both prokaryotic and eukaryotic marine microbes, (2) microbes capable of transporting osmolytes but lacking complete synthesis and/or breakdown pathways, and (3) osmolytes whose synthesis and/or breakdown appears to be specialized and is limited to a subset of organisms. The analysis clearly demonstrates that the marine microbial loop has the genetic potential to actively recycle osmolytes and that this abundant group of small metabolites may function as a significant source of nutrients through exchange among diverse microbial groups that significantly contribute to the cycling of labile carbon.
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