Home > 2019, 38(8) > Phylogenetic diversity of dimethylsulfoniopropionate-dependent demethylase gene dmdA in distantly related bacteria isolated from Arctic and Antarctic marine environments

Citation: Yinxin ZENG. Phylogenetic diversity of dimethylsulfoniopropionate-dependent demethylase gene dmdA in distantly related bacteria isolated from Arctic and Antarctic marine environments. ACTA OCEANOLOGICA SINICA, 2019, 38(8): 64-71. doi: 10.1007/s13131-019-1393-7

2019, 38(8): 64-71. doi: 10.1007/s13131-019-1393-7

Phylogenetic diversity of dimethylsulfoniopropionate-dependent demethylase gene dmdA in distantly related bacteria isolated from Arctic and Antarctic marine environments

1.  Key Laboratory for Polar Science of State Oceanic Administration, Polar Research Institute of China, Shanghai 200136, China

Corresponding author: Yinxin ZENG, yxzeng@yahoo.com

Received Date: 2018-02-23
Web Publishing Date: 2019-08-01

Fund Project: The National Natural Science Foundation of China under contract No. 41476171; the Chinese Polar Environment Comprehensive Investigation and Assessment Program under contract No. CHINARE04-01.

Dimethylsulfoniopropionate (DMSP) is mainly produced by marine phytoplankton as an osmolyte, antioxidant, predator deterrent, or cryoprotectant. DMSP is also an important carbon and sulfur source for marine bacteria. Bacteria may metabolize DMSP via the demethylation pathway involving the DMSP demethylase gene (dmdA) or the cleavage pathway involving several different DMSP lyase genes. Most DMSP released into seawater is degraded by bacteria via demethylation. To test a hypothesis that the high gene frequency of dmdA among major marine taxa results in part from horizontal gene transfer (HGT) events, a total of thirty-one bacterial strains were isolated from Arctic Kongsfjorden seawater in this study. Analysis of 16S rRNA gene sequences showed that, except for strains BSw22118, BSw22131 and BSw22132 belonging to the genera Colwellia, Pseudomonas and Glaciecola, respectively, all bacteria fell into the genus Pseudoalteromonas. DmdA genes were detected in five distantly related bacterial strains, including four Arctic strains (Pseudoalteromonas sp. BSw22112, Colwellia sp. BSw22118, Pseudomonas sp. BSw22131 and Glaciecola sp. BSw22132) and one Antarctic strain (Roseicitreum antarcticum ZS2–28). Their dmdA genes showed significant similarities (97.7%–98.3%) to that of Ruegeria pomeroyi DSS–3, which was originally isolated from temperate coastal seawater. In addition, the sequence of the gene transfer agent (GTA) capsid protein gene (g5) detected in Antarctic strain ZS2–28 exhibited a genetically closely related to that of Ruegeria pomeroyi DSS–3. Among the five tested strains, only Pseudomonas sp. BSw22131 could grow using DMSP as the sole carbon source. The results of this study support the hypothesis of HGT for dmdA among taxonomically heterogeneous bacterioplankton, and suggest a wide distribution of functional gene (i.e., dmdA) in global marine environments.

Key words: dimethylsulfoniopropionate-dependent demethylase gene (dmdA) , horizontal gene transfer , marine bacteria , Arctic , Antarctic


Andreae M O. 1990. Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Marine Chemistry, 30: 1–29.


Bürgermeister S, Georgii H W, Zimmermann R L, et al. 1990. On the biogenic origin of dimethylsulfide: relation between chlorophyll, ATP, organismic DMSP, phytoplankton species, and DMS distribution in Atlantic surface water and atmosphere. Journal of Geophysical Research: Atmosphere, 95(D12): 20607–20615.


Biers E J, Wang Kui, Pennington C, et al. 2008. Occurrence and expression of gene transfer agent genes in marine bacterioplankton. Applied and Environmental Microbiology, 74(10): 2933–2939.


Bullock H A, Luo Haiwei, Whitman W B. 2017. Evolution of dimethylsulfoniopropionate metabolism in marine phytoplankton and bacteria. Frontiers in Microbiology, 8: 637.


Charlson R J, Lovelock J E, Andreae M O, et al. 1987. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature, 326(6114): 655–661.


Cui Yingshun, Suzuki S, Omori Y, et al. 2015. Abundance and distribution of dimethylsulfoniopropionate degradation genes and the corresponding bacterial community structure at dimethyl sulfide hot spots in the tropical and subtropical Pacific Ocean. Applied and Environmental Microbiology, 81(12): 4184–4194.


Curson A R J, Todd J D, Sullivan M J, et al. 2011. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nature Reviews Microbiology, 9(12): 849–859.


Fu Yunyun, MacLeod D M, Rivkin R B, et al. 2010. High diversity of Rhodobacterales in the subarctic North Atlantic Ocean and gene transfer agent protein expression in isolated strains. Aquatic Microbial Ecology, 59(3): 283–293.


Fuhrman J A, Lee S H, Masuchi Y, et al. 1994. Characterization of marine prokaryotic communities via DNA and RNA. Microbial Ecology, 28(2): 133–145.


González J M, Covert J S, Whitman W B, et al. 2003. Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. International Journal of Systematic and Evolutionary Microbiology, 53(5): 1261–1269.


González J M, Kiene R P, Moran M A. 1999. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Applied and Environmental Microbiology, 65(9): 3810–3819


Guillard R R L, Ryther J H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 8(2): 229–239.


Herlemann D P R, Woelk J, Labrenz M, et al. 2014. Diversity and abundance of " Pelagibacterales” (SAR11) in the Baltic Sea salinity gradient. Systematic and Applied Microbiology, 37(8): 601–604.


Hollibaugh J T, Bano N, Ducklow H W. 2002. Widespread distribution in polar oceans of a 16S rRNA gene sequence with affinity to Nitrosospira-like ammonia-oxidizing bacteria. Applied and Environmental Microbiology, 68(3): 1478–1484.


Howard E C, Henriksen J R, Buchan A, et al. 2006. Bacterial taxa that limit sulfur flux from the ocean. Science, 314(5799): 649–652.


Howard E C, Sun Shulei, Biers E J, et al. 2008. Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environmental Microbiology, 10(9): 2397–2410.


Howard E C, Sun Shulei, Reisch C R, et al. 2011. Changes in dimethylsulfoniopropionate demethylase gene assemblages in response to an induced phytoplankton bloom. Applied and Environmental Microbiology, 77(2): 524–531.


Huber T, Faulkner G, Hugenholtz P. 2004. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics, 20(14): 2317–2319.


Johnston A W B, Green R T, Todd J D. 2016. Enzymatic breakage of dimethylsulfoniopropionate—a signature molecule for life at sea. Current Opinion in Chemical Biology, 31: 58–65.


Johnston A W B, Todd J D, Sun Lei, et al. 2008. Molecular diversity of bacterial production of the climate-changing gas, dimethyl sulphide, a molecule that impinges on local and global symbioses. Journal of Experimental Botany, 59(5): 1059–1067.


Karsten U, Kück K, Vogt C, et al. 1996. Dimethylsulfoniopropionate production in phototrophic organisms and its physiological functions as a cryoprotectant. In: Kiene R P, Visscher P T, Keller M D, et al., eds. Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds. New York: Plenum Press, 143–153


Keller M D. 1989. Dimethyl sulfide production and marine phytoplankton: the importance of species composition and cell size. Biological Oceanography, 6(5–6): 375–382.


Kiene R P. 1990. Dimethyl sulfide production from dimethylsulfoniopropionate in coastal seawater samples and bacterial cultures. Applied and Environmental Microbiology, 56(11): 3292–3297


Kiene R P, Linn L J. 2000. Distribution and turnover of dissolved DMSP and its relationship with bacterial production and dimethylsulfide in the Gulf of Mexico. Limnology and Oceanography, 45(4): 849–861.


Kiene R P, Linn L J, Bruton J A. 2000. New and important roles for DMSP in marine microbial communities. Journal of Sea Research, 43(3–4): 209–224.


Kiene R P, Linn L J, González J, et al. 1999. Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Applied and Environmental Microbiology, 65(10): 4549–4558


Kirst G O, Thiel C, Wolff H, et al. 1990. Dimethylsulfoniopropionate (DMSP) in icealgae and its possible biological role. Marine Chemistry, 35(1–4): 381–388.


Lang A S, Beatty J T. 2007. Importance of widespread gene transfer agent genes in α-proteobacteria. Trends in Microbiology, 15(2): 54–62.


Lang A S, Zhaxybayeva O, Beatty J T. 2012. Gene transfer agents: phage-like elements of genetic exchange. Nature Reviews Microbiology, 10(7): 472–482.


Marrs B. 1974. Genetic recombination in Rhodopseudomonas capsulata. Proceedings of the National Academy of Sciences of the United States of America, 71(3): 971–973.


McDaniel L D, Young E, Delaney J, et al. 2010. High frequency of horizontal gene transfer in the oceans. Science, 330(6000): 50.


Moran M A, Reisch C R, Kiene R P, et al. 2012. Genomic insights into bacterial DMSP transformations. Annual Review of Marine Science, 4: 523–542.


Pawlowski J, Fahrni J, Lecroq B, et al. 2007. Bipolar gene flow in deep-sea benthic foraminifera. Molecular Ecology, 16(19): 4089–4096.


Pommier T, Pinhassi J, Hagström A. 2005. Biogeographic analysis of ribosomal RNA clusters from marine bacterioplankton. Aquatic Microbial Ecology, 41(1): 79–89.


Reisch C R, Moran M A, Whitman W B. 2008. Dimethylsulfoniopropionate-dependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi. Journal of Bacteriology, 190(24): 8018–8024.


Reisch C R, Stoudemayer M J, Varaljay V A, et al. 2011. Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature, 473(7346): 208–211.


Ripp S, Miller R V. 1995. Effects of suspended particulates on the frequency of transduction among Pseudomonas aeruginosa in a freshwater environment. Applied and Environmental Microbiology, 61(4): 1214–1219


Salgado P, Kiene R, Wiebe W, et al. 2014. Salinity as a regulator of DMSP degradation in Ruegeria pomeroyi DSS-3. Journal of Microbiology, 52(11): 948–954.


Sambrook J, Russell D W. 2001. Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press


Schwartz S E, Andreae M O. 1996. Uncertainty in climate change caused by aerosols. Science, 272(5265): 1121.


Shaw G E. 1983. Bio-controlled thermostasis involving the sulfur cycle. Climatic Change, 5(3): 297–303.


Solioz M, Marrs B. 1977. The gene transfer agent of Rhodopseudomonas capsulata: purification and characterization of its nucleic acid. Archives of Biochemistry and Biophysics, 181(1): 300–307.


Sun Jing, Todd J D, Thrash J C, et al. 2016. The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol. Nature Microbiology, 1(8): 16065.


Sunda W, Kieber D J, Kiene R P, et al. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature, 418(6895): 317–320.


Tamura K, Peterson D, Peterson N, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731–2739.


Thompson J D, Higgins D G, Gibson T J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22): 4673–4680.


Turner S M, Nightingale P D, Broadgate W, et al. 1995. The distribution of dimethyl sulphide and dimethylsulphoniopropionate in Antarctic waters and sea ice. Deep Sea Research Part II: Topical Studies in Oceanography, 42(4–5): 1059–1080.


Vettori C, Stotzky G, Yoder M, et al. 1999. Interaction between bacteriophage PBS1 and clay minerals and transduction of Bacillus subtilis by clay-phage complexes. Environmental Microbiology, 1(4): 347–355.


Visscher P T, Diaz M R, Taylor B F. 1992. Enumeration of bacteria which cleave or demethylate dimethylsulfoniopropionate in the Caribbean Sea. Marine Ecology Progress Series, 89: 293–296.


Weinbauer M G. 2004. Ecology of prokaryotic viruses. FEMS Microbiology Reviews, 28(2): 127–181.


Wolfe G V, Steinke M, Kirst G O. 1997. Grazing-activated chemical defence in a unicellular marine alga. Nature, 387(6636): 894–897.


Yen H C, Hu N T, Marrs B L. 1979. Characterization of the gene transfer agent made by an overproducer mutant of Rhodopseudomonas capsulata. Journal of Molecular Biology, 131(2): 157–168.


Yu Yong, Yan Shulin, Li Huirong, et al. 2011. Roseicitreum antarcticum gen. nov., sp. nov., an aerobic bacteriochlorophyll a-containing alphaproteobacterium isolated from Antarctic sandy intertidal sediment. International Journal of Systematic and Evolutionary Microbiology, 61(9): 2173–2179.


Zeng Yinxin, Liu Wenqi, Li Huirong, et al. 2007. Effect of restriction endonucleases on assessment of biodiversity of cultivable polar marine planktonic bacteria by amplified ribosomal DNA restriction analysis. Extremophiles, 11(5): 685–692.


Zeng Yinxin, Qiao Zongyun, Yu Yong, et al. 2016. Diversity of bacterial dimethylsulfoniopropionate degradation genes in surface seawater of Arctic Kongsfjorden. Scientific Reports, 6: 33031.


Zhao Yanlin, Wang Kui, Budinoff C, et al. 2008. Gene transfer agent (GTA) genes reveal diverse and dynamic Roseobacter and Rhodobacter populations in the Chesapeake bay. The ISME Journal, 3(3): 364–373.


Zhen WANG, Yang LI, Xuezheng LIN. Transcriptome analysis of the Antarctic psychrotrophic bacteriumPsychrobacter sp. G in response to temperature stress. ACTA OCEANOLOGICA SINICA, 2017, 36(2): 78-87. doi: 10.1007/s13131-016-0956-0


Ping CHEN, Jinping ZHAO. Variation of sea ice extent in different regions of the Arctic Ocean. ACTA OCEANOLOGICA SINICA, 2017, 36(8): 9-19. doi: 10.1007/s13131-016-0886-x


Zhongqiao LI, Xinyi WANG, Haiyan JIN, Zhongqiang JI, Youcheng BAI, Jianfang CHEN. Variations in organic carbon loading of surface sediments from the shelf to the slope of the Chukchi Sea, Arctic Ocean. ACTA OCEANOLOGICA SINICA, 2017, 36(8): 131-136. doi: 10.1007/s13131-017-1026-y


Haili Li, Changqing Ke, Qinghui Zhu, Su Shu. Spatial-temporal variations in net primary productivity in the Arctic from 2003 to 2016. ACTA OCEANOLOGICA SINICA, 2019, 38(8): 111-121. doi: 10.1007/s13131-018-1274-5


Jian WANG, Zhaohui WANG, Jiangang ZHAO. Isolation, characterization and implications of the bacterial communities associated with established cultures of Chattonella marina (Raphidophyceae) and Skeletonema costatum (Bacillariophyceae). ACTA OCEANOLOGICA SINICA, 2019, 38(1): 128-135. doi: 10.1007/s13131-019-1379-5


Lijian SHI, Mingming LI, Chaofang ZHAO, Zhixiong WANG, Yingni SHI, Juhong ZOU, Tao ZENG. Sea ice extent retrieval with HY-2A scatterometer data and its assessment. ACTA OCEANOLOGICA SINICA, 2017, 36(8): 76-83. doi: 10.1007/s13131-017-1022-2


Heshan LIN, Kun LIU, Jianjun WANG, Yaqin HUANG, Zhong LI, Junhui LIN, Xuebao HE, Shuyi ZHANG, Jianfeng MOU, Yu WANG, Bingpeng XING. Spatial pattern of macrobenthic communities along a shelf-slope-basin transect across the Bering Sea. ACTA OCEANOLOGICA SINICA, 2018, 37(6): 72-81. doi: 10.1007/s13131-018-1192-6


Wei ZHAO, Jingjing WANG, Yajie LIANG, Zhiyong HUANG. Development of a 16S rRNA gene-based microarray for the detection of marine bacterioplankton community. ACTA OCEANOLOGICA SINICA, 2017, 36(10): 106-114. doi: 10.1007/s13131-017-1055-6


Xiaotian Han, Shuai Wang, Li Zheng, Wanshun Liu. Identification and characterization of a delta-12 fatty acid desaturase gene from marine microalgae Isochrysis galbana. ACTA OCEANOLOGICA SINICA, 2019, 38(2): 107-113. doi: 10.1007/s13131-019-1354-1


Guoping ZHU, Haiting ZHANG, Qi SONG, Yang YANG, Shaoqin WANG, Qingyuan YANG. Inferring trophic variation for Antarctic krill (Euphausia superba) in the Antarctic Peninsula from the austral fall to early winter using stable isotope analysis. ACTA OCEANOLOGICA SINICA, 2018, 37(6): 90-95. doi: 10.1007/s13131-018-1176-6


Wenjun YAO, Jiuxin SHI. Pacific-Indian interocean circulation of the Antarctic Intermediate Water around South Australia. ACTA OCEANOLOGICA SINICA, 2017, 36(7): 4-14. doi: 10.1007/s13131-017-1078-z


Ye ZHANG, Chaolun LI, Guang YANG, Yanqing WANG, Zhencheng TAO, Yongshan ZHANG, Aijun WANG. Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: a stable isotope analysis. ACTA OCEANOLOGICA SINICA, 2017, 36(12): 67-78. doi: 10.1007/s13131-017-1049-4


Yanshuo WANG, Fei HUANG, Tingting FAN. Spatio-temporal variations of Arctic amplification and their linkage with the Arctic oscillation. ACTA OCEANOLOGICA SINICA, 2017, 36(8): 42-51. doi: 10.1007/s13131-017-1025-z


Na LIU, Bin KONG, Lina LIN, Yan HE, Yanguang LIU, Longshan LIN, Tao ZHANG, Jianfang CHEN. Chinese seventh Arctic scientific expedition. ACTA OCEANOLOGICA SINICA, 2017, 36(3): 115-116. doi: 10.1007/s13131-017-1044-9


Libin ZHANG, Qiming FENG, Lina SUN, Yan FANG, Dongxue XU, Tao ZHANG, Hongsheng YANG. Differential gene expression in the body wall of the sea cucumber (Apostichopus japonicus) under strong lighting and dark conditions. ACTA OCEANOLOGICA SINICA, 2018, 37(5): 54-66. doi: 10.1007/s13131-017-1101-4


Panpan Chen, Jun Song, Xin Shen, Yuefeng Cai, Ka Hou Chu, Yongqi Li, Mei Tian. Mitochondrial genome of Chthamalus challengeri (Crustacea: Sessilia): gene order comparison within Chthamalidae and phylogenetic consideration within Balanomorpha. ACTA OCEANOLOGICA SINICA, 2019, 38(6): 25-31. doi: 10.1007/s13131-019-1355-0


Quanrui Chen, Jingfeng Fan, Jie Su, Hongxia Ming, Zhihao Sun, Mengfei Li, Xiaohui Zhao, Yantao Wang, Yingxue Zhang, Huizhen Zhang, Yuan Jin, Xiaowan Ma, Bin Wang. Spatial distribution characteristics of bacterial community structure and gene abundance in sediments of the Bohai Sea. ACTA OCEANOLOGICA SINICA, 2019, 38(12): 1-10.


Wenjie Yan, Jiao Liu, Samphal Seng, Bin Zhou, Kuke Ding. Cloning, characterization and expression analysis of a microsomal glutathione S-transferase gene from the seagrass Zostera marina. ACTA OCEANOLOGICA SINICA, 2019, 38(10): 111-115. doi: 10.1007/s13131-019-1429-z


Lixin WEI, Ting QIN, Cheng LI. Seasonal and inter-annual variations of Arctic cyclones and their linkage with Arctic sea ice and atmospheric teleconnections. ACTA OCEANOLOGICA SINICA, 2017, 36(10): 1-7. doi: 10.1007/s13131-017-1117-9


Dawei Gui, Xiaoping Pang, Ruibo Lei, Xi Zhao, Jia Wang. Changes in sea ice kinematics in the Arctic outflow region and their associations with Arctic Northeast Passage accessibility. ACTA OCEANOLOGICA SINICA, 2019, 38(8): 101-110. doi: 10.1007/s13131-019-1451-1

  • PDF Downloads()
  • Abstract Views()
  • HTML Views()

Figures And Tables

Phylogenetic diversity of dimethylsulfoniopropionate-dependent demethylase gene dmdA in distantly related bacteria isolated from Arctic and Antarctic marine environments

Yinxin ZENG