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Acrylate protects a marine bacterium from grazing by a ciliate predator

Abstract

Cleavage of dimethylsulfoniopropionate (DMSP) can deter herbivores in DMSP-producing eukaryotic algae; however, it is unclear whether a parallel defence mechanism operates in marine bacteria. Here we demonstrate that the marine bacterium Puniceibacterium antarcticum SM1211, which does not use DMSP as a carbon source, has a membrane-associated DMSP lyase, DddL. At high concentrations of DMSP, DddL causes an accumulation of acrylate around cells through the degradation of DMSP, which protects against predation by the marine ciliate Uronema marinum. The presence of acrylate can alter the grazing preference of U. marinum to other bacteria in the community, thereby influencing community structure.

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Fig. 1: The predation rates and ratios of U. marinum preying on the wild-type P. antarcticum SM1211 and ΔdddL mutant in the presence and absence of DMSP.
Fig. 2: Decrease of protozoan predation preference to P. antarcticum SM1211 in the presence of DMSP.

Data availability

Sequence data that support the findings of this study are available in the supplementary information. Source data are provided with this paper.

Code availability

No customized code was used.

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Acknowledgements

We thank Z.-F. Li and H.-Y. Yu from the State Key Laboratory of Microbial Technology at Shandong University for help and guidance in flow cytometry and laser-scanning confocal microscopy, respectively. We thank I. Hands-Portman and the Imaging Suite at the School of Life Sciences, University of Warwick for providing assistance with the use of confocal microscopy. This work was supported by the National Key Research and Development Program of China (grant no. 2018YFC1406700), the National Science Foundation of China (grant nos. 91851205, 31630012, U1706207, 31870052, 3217010695 and 41706152), the Fundamental Research Funds for the Central Universities (grant no. 202172002), Major Scientific and Technological Innovation Project (MSTIP) of Shandong Province (grant no. 2019JZZY010817) and the Program of Shandong for Taishan Scholars (tspd20181203).

Author information

Affiliations

Authors

Contributions

Z.-J.T. designed and performed most of the experiments and data interpretation. P.W. conceived the project and performed protein purification. X.-L.C. directed the study. R.G. performed the intraspecies selective predation experiments and data interpretation. C.-Y.L. helped with experiments and data interpretation. S.-B.Z. and J.G. helped with experiments. K.-W.X. modelled the micropatch diffusion dynamic of acrylate. L.H. and C.W. helped in constructing the microfluidic biochip. L.H. and C.W. helped in constructing the microfluidic biochip. Z.-J.T. and X.-L.C. wrote the manuscript. D.J.S. provided input in the selective predation experiments and critically revised the manuscript. Y.C. directed the study and did a critical revision of the manuscript for important intellectual content. Y.-Z.Z. conceived the project, designed the experiments and directed the study.

Corresponding author

Correspondence to Yu-Zhong Zhang.

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The authors declare no competing interests.

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Peer review information Nature Microbiology thanks Virginia Edgcomb and the other, anonymous, reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Characterization of strain SM1211 and various mutant strains.

a, Growth of strain SM1211 cultured with 1 mM succinate, 1 mM DMSP or 1 mM acrylate as the sole carbon source. Control, no carbon source was added. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. b, c, Detection of DMS (b, indicated by black arrows) and extracellular acrylate (c, indicated by black arrows) produced by the wild-type strain SM1211, the ΔdddL mutant, and the complemented mutant strain ZH171 (DMS and acrylate produced at the rate of 1.65 ± 0.02 × 10−5 μΜ s−1 μg−1 and 2.62 ± 1.57 × 10−13 μΜ s−1 cell−1, respectively). The dashed line presents the direction of z-axis. d, Bacterial growth and extracellular acrylate concentration when strain SM1211 was cultured in a minimal medium supplemented with 1 mM acrylate. The line indicates the OD600 values of bacterial growth, and the bar indicates the concentration of acrylate in the culture medium (n = 3). Control, no bacteria added in the culture medium with 1 mM acrylate. All experiments were carried out in three replicates. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. e, Tolerance of strain SM1211 to different concentrations of acrylate (1-10 mM) when cultivated in the 2216E medium. Data are presented as mean values +/- standard deviation. Error bars represent the standard deviation of triplicate experiments. f, Expression levels of the dddL gene in strain SM1211 induced by 1 mM DMSP, 1 mM acrylate or 1 mM 3-hydroxypropionate (3-HP). Strain SM1211 cultured in minimal medium with 10 mM succinate as the sole carbon source was used as control. The rpoD gene was used to normalise the expression of dddL. Expression levels of dddL in strain SM1211 with different inducers at each sampling time were normalized by that without an inducer. All experiments were carried out in three replicates. Error bars represent standard deviation of triplicate experiments. g, Growth of strains SM1211, ΔdddL, ZH171 (complemented mutant), and ZH172 (ΔdddL harboring the vector pBBR1MCS-4) cultured in the 2216E medium at 25 °C. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. h, Detection of the DMSP cleavage activities of strains ZH173 (ΔdddL harboring pBBR1MCS-4 which carries the promoter and coding sequence of DddL fused with sfGFP) and ZH174 (ΔdddL harboring pBBR1MCS-4 which carries the coding sequence of sfGFP) by measuring the production of acrylate via HPLC. i, Fluorescence intensity of proteins extracted from the membrane (M), periplasmic (P) and cytoplasmic (C) fractions of strain ZH173. The majority of the fluorescence intensity was in the membrane fraction as denoted by the peak at the excitation wavelength of 480 nm. j, DMSP cleavage activity of proteins extracted from the membrane (M), periplasmic (P) and cytoplasmic (C) fractions of strain ZH173 (n = 3). All experiments were carried out in three replicates. Data are presented as mean values +/- standard deviation, and error bars represent standard deviation of triplicate experiments. k, Localization of the DddL-sfGFP fusion protein (DddL-sfGFP) in strain ZH173. White arrows indicate the location of DddL. Scale bar = 2 μm. l, The sfGFP protein expressed in strain ZH174. The sfGFP protein distributes evenly in the cytoplasm of cells. Scale bar = 2 μm. m, The DddL-sfGFP fusion protein expressed in strain ZH175 (strain SM1211 harboring pBBR1MCS-4 which carries the promoter and coding sequence of DddL fused with sfGFP). The DddL-sfGFP fusion protein is localized at the pole of cell. White arrows indicate the location of DddL. Scale bar = 2 μm. Each picture is a representative of at least three repeats (km).

Source data

Extended Data Fig. 2 DMSP cleavage activity of purified DddL.

a, SDS-polyacrylamide gel electrophoresis assay of the purified DddL protein. The DddL protein is indicated by a black arrow. M, protein molecular weight marker. Each picture is a representative of at least three repeats. b, SDS-polyacrylamide gel electrophoresis and western blot assays of the overexpression profile of DddL in the membrane and the cytoplasmic fractions. Marker, protein molecular weight marker with the unit of kDa. Me, proteins in the membrane; Cyto, proteins in the cytoplasm; DddL, the purified DddL. WB, western blot. White arrows indicate the DddL protein band. Each picture is a representative of at least three repeats. c, Detection of the DMSP cleavage activity of the purified DddL protein by measuring the production of acrylate via HPLC. The black arrow indicates the absorption peak of acrylate at 214 nm. The dashed line presents the direction of z-axis. d, The effect of pH on DddL activity. The activity of DddL at pH 9.0 was defined as 100%. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. e, The effect of temperature on DddL activity. The activity of DddL at 30 °C was defined as 100%. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. fh, Enzymatic kinetic parameters for DMSP cleavage by DddL. A linear fit curve measured at 4 °C, pH 8.0 (f), and non-linear fit curves measured at 18 °C, pH 8.0 (g), and 30 °C, pH 9.0 (h).

Source data

Extended Data Fig. 3 The ecological effects of acrylate and DMSP on U. marinum.

ad, Cells stained with 5-(4,6-dichlorotriazinyl) aminofluorescein (DTAF). SM1211 (a), ΔdddL (b), ZH171 (c), and P. arctica (d). The images show that the cells are uniformly stained by DTAF and are similar in size. Scale bars = 5 μm. Each picture is a representative of at least three repeats. e, The chemotactic response of U. marinum to DMSP. The times of ciliates attracted into the microchannels were recorded for 10 min in the presence or absence of 500 μM DMSP (n = 1232 and 249, P value = 1.00E-06), and the ciliates detained in microchannels were counted after 10 min (n = 114 and 1, P value = 3.00E-04). The boxes in the plot are bound by the 25% to 75% quartile proportions with the thick blue line being the median value. Red dots indicate average values. A two-sided t-test was used to assess statistically significant differences between samples; ***, P < 0.001; n, sample size. f, The chemotactic response of U. marinum to DMS. The times of ciliates attracted into the microchannels were recorded for 10 min in the presence or absence of 100 μM DMS (n = 605 and 243, P value = 0.007), and the ciliates detained in microchannels were counted after 10 min (n = 57 and 12, P value = 0.005). A two-sided t-test was used to assess statistically significant differences between samples; **, P < 0.01; n, sample size. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. g, Growth curves of U. marinum preying on ΔdddL in the presence (grey) or absence (black) of 500 μM DMS. h, i, Growth curves of U. marinum preying on strain SM1211 (h) and its mutant ΔdddL (i) in the presence (grey) or absence (black) of 70 μM acrylate. The dotted red lines indicate the concentration of acrylate in the system with DMSP. No acrylate was detected in the system without DMSP. The acrylate concentration on the y-axis is shown in red. All experiments were carried out in technical triplicates. j, Effect of the addition of 0 (red), 70 μM (blue), 500 μM (orange) or 1 mM (grey) acrylate on the growth of U. marinum. Inactivated P. arctica was used as prey for U. marinum. No acrylate was detected in the system without acrylate. All experiments were carried out in technical triplicates.

Source data

Extended Data Fig. 4 The selective predation of U. marinum on different prey.

a, Confocal micrographs of the food vacuoles in U. marinum preying on the co-incubated strain SM1211 and ΔdddL in the absence or presence of 500 μM DMSP. Strain SM1211 and ΔdddL were labelled with sfGFP and mCherry, respectively, and the nucleus of U. marinum was stained by DAPI. Scale bars = 20 μm. Each picture is a representative of at least three repeats. b, The effect of acrylate on the viability of ΔdddL measured by colony forming units (CFU). The mix of strains ZH176 (strain SM1211 harboring pBBR1MCS-2 which carries the coding sequence of sfGFP) and ZH177 (ΔdddL harboring pBBR1MCS-5 which carries the coding sequence of mCherry) was also plated on 2216E solid medium containing gentamycin in order to enumerate only ZH177 during the mix. Data are presented as mean values +/- standard deviation. Experiments were carried out in three replicates and error bars represent standard deviation. c, The tolerance of P. arctica to different concentrations of acrylate (1-10 mM) when cultivated in the 2216E medium. Data are presented as mean values +/- standard deviation. Error bars represent the standard deviation of triplicate experiments. d-f, Growth of P. arctica (d), Marinobacter antarcticus 4-2 (e) and Polaribacter sp. K15 (f) cultured with 1 mM succinate, 1 mM DMSP or 1 mM acrylate as the sole carbon source. Control, no carbon source was added. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. g-h, The tolerance of Marinobacter antarcticus 4-2 (g) and Polaribacter sp. K15 (h) to different concentrations of acrylate (1-10 mM) when cultivated in the 2216E medium. Data are presented as mean values +/- standard deviation. Error bars represent the standard deviation of triplicate experiments. i, Prey abundance ratios in the presence or absence of 500 μM DMSP with or without U. marinum after 72 h incubation (n = 3). Four bacterial species (strain SM1211 or the mutant ΔdddL with P. arctica, Marinobacter antarcticus 4-2 and Polaribacter sp. K15) were utilized as prey for U. marinum. The dotted lines indicate the original prey abundance ratio at 0 h. Approximately 300 ciliate cells were added to the predation system and the ratio of ciliates to bacteria was ~1:106. All experiments were carried out in three replicates. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments.

Source data

Extended Data Fig. 5 The phylogenetic and geographic distribution of bacteria containing the dddL gene.

a, Marine bacteria harboring the dddL gene are dominated by α-proteobacteria and are widely distributed in oceanic environments. Blue dots indicate the sampling stations of these species. The circular tree represents a neighbor-joining tree that was built based on the 16S rRNA gene sequences of dddL-containing strains. EQ, equator. b, A neighbor-joining tree was built based on DddL amino acid sequences. Strains from Alphaproteobacteria, Gammaproteobacteria, Deltaproteobacteria, and Actinobacteria are shown in red, grey, orange and blue, respectively. Arrows connect donors and recipients, and the arrow colors correspond to the donors. c, Statistics of dddL gene abundance in metagenomic samples from various marine sources in the IMG/M database. ND, not detected.

Source data

Extended Data Fig. 6 The Abundance of U. marinum preying on other strains containing DMSP lyases.

a, Growth of Ruegeria lacuscaerulensis ITI-1157 cultured with 1 mM succinate, 1 mM DMSP or 1 mM acrylate as the sole carbon source. Control, no carbon source was added. Data are presented as mean values +/- standard deviation. Error bars represent standard deviation of triplicate experiments. b, Detection of DMS (indicated by black arrows) produced by strain ITI-1157. The dashed line presents the direction of z-axis. cf, Abundance of ciliates after feeding on dddL-containing strains for 60 h in the presence or absence of 500 μM DMSP. 25204, Roseivivax isoporae LMG 25204 (c); B108, Roseovarius indicus strain B108 (d); 12614, Labrenzia aggregata IAM 12614 (e); 17023, Labrenzia marina DSM 17023 (f). g, Growth curves of U. marinum preying on strain ITI-1157 in the presence or absence of 500 μM DMSP.

Source data

Extended Data Fig. 7 Accumulated acrylate protects Puniceibacterium antarcticum SM1211 from protozoan predation.

a, Spatio-temporal variation of the acrylate concentration. Acrylate produced by a 1-μm radius SM1211 cell, and time elapsed after acrylate production. b, The proposed chemical defense strategy adopted by strain SM1211 with DMSP as the precursor compound. DMSP produced mostly by phytoplankton can be released into the environment via grazing or viral lysis. The membrane-localized DddL of strain SM1211 cleaves DMSP to generate acrylate, which forms a defense shelter to protect against the predator Uronema marinum which are attracted by DMSP and the co-generated DMS. The defense function of the acrylate shelter counteracts the foraging response of U. marinum to strain SM1211 and transfers grazing pressure to non-dddL-containing strains, reducing population losses of strain SM1211. OM, outer membrane; IM, inner membrane.

Supplementary information

Supplementary Information

Supplementary Figs. 1–3, Tables 1–11 and references.

Reporting Summary

Supplementary Table 12

The information of bacterial strains containing homology of DddL.

Supplementary Table 13

The distribution of dddL gene in different types of metagenomic sample.

Source data

Source Data Fig. 1

Original images for Fig. 1a.

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Statistical source data for Fig. 1b,c.

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Original images for Fig. 2a.

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Statistical source data for Fig. 2b–d.

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Statistical source data for Extended Data Fig. 1a,d–g,i,j.

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Original images for Extended Data Fig. 1b,c,h,k–m.

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Unprocessed gel for Extended Data Fig. 2a, unprocessed western blots for Extended Data Fig. 2b and original images for Extended Data Fig. 2c.

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Statistical source data for Extended Data Fig. 2d–h.

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Original images for Extended Data Fig. 3a–d.

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Statistical source data for Extended Data Fig. 3e–g.

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Statistical source data for Extended Data Fig. 6a,c–g.

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Original images for Extended Data Fig. 6b.

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Teng, ZJ., Wang, P., Chen, XL. et al. Acrylate protects a marine bacterium from grazing by a ciliate predator. Nat Microbiol 6, 1351–1356 (2021). https://doi.org/10.1038/s41564-021-00981-1

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