Family-level diversity of extracellular proteases of sedimentary bacteria from the South China Sea

Yang Jinyu; Feng Yangyang; Chen Xiulan; Xie Binbin; Zhang Yuzhong; Shi Mei; Zhang Xiying

doi:10.1007/s13131-019-1391-9

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Article Navigation > Acta Oceanologica Sinica > 2019 > 38(12): 73-83

Yang Jinyu, Feng Yangyang, Chen Xiulan, Xie Binbin, Zhang Yuzhong, Shi Mei, Zhang Xiying. Family-level diversity of extracellular proteases of sedimentary bacteria from the South China Sea[J]. Acta Oceanologica Sinica, 2019, 38(12): 73-83. doi: 10.1007/s13131-019-1391-9

Citation:

Yang Jinyu, Feng Yangyang, Chen Xiulan, Xie Binbin, Zhang Yuzhong, Shi Mei, Zhang Xiying. Family-level diversity of extracellular proteases of sedimentary bacteria from the South China Sea[J]. Acta Oceanologica Sinica, 2019, 38(12): 73-83. doi: 10.1007/s13131-019-1391-9

Citation:

Yang Jinyu, Feng Yangyang, Chen Xiulan, Xie Binbin, Zhang Yuzhong, Shi Mei, Zhang Xiying. Family-level diversity of extracellular proteases of sedimentary bacteria from the South China Sea[J]. Acta Oceanologica Sinica, 2019, 38(12): 73-83. doi: 10.1007/s13131-019-1391-9

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Family-level diversity of extracellular proteases of sedimentary bacteria from the South China Sea

doi: 10.1007/s13131-019-1391-9

1.
State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao 266237, China;Institute of Agro-Food Science and Technology, Shandong Academy of Agricultural Sciences/Key Laboratory of Agro-Products Processing Technology of Shandong Province/Key Laboratory of Novel Food Resources Processing, Ministry of Agriculture and Rural Affairs, Jinan 250100, China
2.
State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao 266237, China
3.
State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao 266237, China;Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China;College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China

Received Date: 2018-12-07

Abstract

Abstract

Protease-producing bacteria and their extracellular proteases are key players in degrading organic nitrogen to drive marine nitrogen cycling and yet knowledge on both of them is still very limited. This study screened protease-producing bacteria from the South China Sea sediments and analyzed the diversity of their extracellular proteases at the family level through N-terminal amino acid sequencing. Results of the 16S rRNA gene sequence analysis showed that all screened protease-producing bacteria belonged to the class Gammaproteobacteria and most of them were affiliated with different genera within the orders Alteromonadales and Vibrionales. The N-terminal amino acid sequence analysis for fourteen extracellular proteases from fourteen screened bacterial strains revealed that all these proteases belonged to the M4 family of metalloproteases or the S8 family of serine proteases. This study presents new details on taxa of marine sedimentary protease-producing bacteria and types of their extracellular proteases, which will help to comprehensively understand the process and mechanism of the microbial enzymatic degradation of marine sedimentary organic nitrogen.
- protease-producing bacteria,
- diversity,
- extracellular proteases,
- protease families,
- N-terminal amino acid sequencing,
- South China Sea

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References(47)

References

Arnosti C. 2011. Microbial extracellular enzymes and the marine carbon cycle. Annual Review of Marine Science, 3:401-425, doi: 10.1146/annurev-marine-120709-142731

Arnosti C, Bell C, Moorhead D L, et al. 2014. Extracellular enzymes in terrestrial, freshwater, and marine environments:perspectives on system variability and common research needs. Biogeochemistry, 117(1):5-21, doi: 10.1007/s10533-013-9906-5

Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology, 5(10):782-791, doi: 10.1038/nrmicro1747

Boetius A, Lochte K. 1994. Regulation of microbial enzymatic degradation of OM in deep-sea sediments. Marine Ecology Progress, 104:299-307, doi: 10.3354/meps104299

Bridoux M C, Neibauer J, Ingalls A E, et al. 2015. Suspended marine particulate proteins in coastal and oligotrophic waters. Journal of Marine Systems, 143:39-48, doi: 10.1016/j.jmarsys.2014.10.014

Chen Xiulan, Xie Binbin, Bian Fei, et al. 2009. Ecological function of myroilysin, a novel bacterial M12 metalloprotease with elastinolytic activity and a synergistic role in collagen hydrolysis, in biodegradation of deep-sea high-molecular-weight organic nitrogen. Applied and Environmental Microbiology, 75(7):1838-1844, doi: 10.1128/AEM.02285-08

Chen Xiulan, Xie Binbin, Lu Jingtao, et al. 2007. A novel type of subtilase from the psychrotolerant bacterium Pseudoalteromonas sp. SM9913:catalytic and structural properties of deseasin MCP-01. Microbiology, 153(7):2116-2125, doi: 10.1099/mic.0.2007/006056-0

Chen Xiulan, Zhang Yuzhong, Gao Peiji, et al. 2003. Two different proteases produced by a deep-sea psychrotrophic bacterial strain, Pseudoaltermonas sp. SM9913. Marine Biology, 143(5):989-993, doi: 10.1007/s00227-003-1128-2

Chenna R, Sugawara H, Koike T, et al. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research, 31(13):3497-3500, doi: 10.1093/nar/gkg500

Fabiano M, Danovaro R. 1998. Enzymatic activity, bacterial distribution, and organic matter composition in sediments of the ross sea (Antarctica). Applied and Environmental Microbiology, 64(10):3838-3845

Gao Xiang, Wang Jue, Yu Daqi, et al. 2010. Structural basis for the autoprocessing of zinc metalloproteases in the thermolysin family. Proceedings of the National Academy of Sciences of the United States of America, 107(41):17569-17574, doi: 10.1073/pnas.1005681107

Geng Ce, Nie Xiangtao, Tang Zhichao, et al. 2016. A novel serine protease, Sep1, from Bacillus firmus DS-1 has nematicidal activity and degrades multiple intestinal-associated nematode proteins. Scientific Reports, 6:25012, doi: 10.1038/srep25012

He Hailun, Guo Jun, Chen Xiulan, et al. 2012. Structural and functional characterization of mature forms of metalloprotease E495 from Arctic sea-ice bacterium Pseudoalteromonas sp. SM495. PLoS One, 7(4):e35442, doi: 10.1371/journal.pone.0035442

Herbert R A. 1999. Nitrogen cycling in coastal marine ecosystems. FEMS Microbiology Reviews, 23(5):563-590, doi: 10.1111/j.1574-6976.1999.tb00414.x

Jørgensen B B, Boetius A. 2007. Feast and famine-microbial life in the deep-sea bed. Nature Reviews Microbiology, 5(10):770-781, doi: 10.1038/nrmicro1745

Jung S Y, Jung Y T, Oh T K, et al. 2007. Photobacterium lutimaris sp. nov., isolated from a tidal flat sediment in Korea. International Journal of Systematic and Evolutionary Microbiology, 57(2):332-336, doi: 10.1099/ijs.0.64580-0

Kessler E, Safrin M, Olson J C, et al. 1993. Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. Journal of Biological Chemistry, 268(10):7503-7508

Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2):111-120, doi: 10.1007/BF01731581

Li Huijuan, Tang Bailu, Shao Xuan, et al. 2016. Characterization of a new S8 serine protease from marine sedimentary Photobacterium sp. A5-7 and the function of its protease-associated domain. Frontiers in Microbiology, 7:2016, doi: 10.3389/fmicb.2016.02016

Li Yan, Wu Chaoya, Zhou Mingyang, et al. 2017. Diversity of cultivable protease-producing bacteria in Laizhou Bay sediments, Bohai Sea, China. Frontiers in Microbiology, 8:405, doi: 10.3389/fmicb.2017.00405

Lloyd K G, Schreiber L, Petersen D G, et al. 2013. Predominant archaea in marine sediments degrade detrital proteins. Nature, 496(7444):215-218, doi: 10.1038/nature12033

Long R A, Azam F. 2001. Antagonistic interactions among marine pelagic bacteria. Applied and Environmental Mircobiology, 67(11):4975-4983, doi: 10.1128/AEM.67.11.4975-4983.2001

Matsuyama H, Sawazaki K, Minami H, et al. 2014. Pseudoalteromonas shioyasakiensis sp. nov., a marine polysaccharide-producing bacterium. International Journal of Systematic and Evolutionary Microbiology, 64(1):101-106, doi: 10.1099/ijs.0.055558-0

Moore E K, Harvey H R, Faux J F, et al. 2014. Electrophoretic extraction and proteomic characterization of proteins buried in marine sediments. Chromatography, 1(4):176-193, doi: 10.3390/chromatography1040176

Nelson P N, Baldock J A. 2005. Estimating the molecular composition of a diverse range of natural organic materials from solid-state ¹³C NMR and elemental analyses. Biogeochemistry, 72(1):1-34, doi: 10.1007/s10533-004-0076-3

Olivera N L, Sequeiros C, Nievas M L. 2007. Diversity and enzyme properties of protease-producing bacteria isolated from sub-Antarctic sediments of Isla de Los Estados, Argentina. Extremophiles, 11(3):517-526, doi: 10.1007/s00792-007-0064-3

Patel A B, Fukami K, Nishijima T. 2001. Extracellular proteolytic activity in the surface sediment of a eutrophic inlet. Microbes and Environments, 16(1):25-35, doi: 10.1264/jsme2.2001.25

Poremba K. 1995. Hydrolytic enzymatic activity in deep-sea sediments. FEMS Microbiology Ecology, 16(3):213-221, doi: 10.1111/fem.1995.16.issue-3

Qin Qilong, Zhang Xiying, Wang Xumin, et al. 2010. The complete genome of Zunongwangia profunda SM-A87 reveals its adaptation to the deep-sea environment and ecological role in sedimentary organic nitrogen degradation. BMC Genomics, 11:247, doi: 10.1186/1471-2164-11-247

Ran Liyuan, Su Hainan, Zhao Guoyan, et al. 2013. Structural and mechanistic insights into collagen degradation by a bacterial collagenolytic serine protease in the subtilisin family. Molecular Microbiology, 90(5):997-1010, doi: 10.1111/mmi.12412

Ran Liyuan, Su Hainan, Zhou Mingyang, et al. 2014. Characterization of a novel subtilisin-like protease myroicolsin from deep sea bacterium Myroides profundi D25 and molecular insight into its collagenolytic mechanism. Journal of Biological Chemistry, 289(9):6041-6053, doi: 10.1074/jbc.M113.513861

Rawlings N D, Barrett A J, Thomas P D, et al. 2018. The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids Research, 46(D1):D624-D632, doi: 10.1093/nar/gkx1134

Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42(Web server issue):W320-W324, doi: 10.1093/nar/gku316

Saitou N, Nei M. 1987. The neighbor-joining method:a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4):406-425, doi: 10.1093/oxfordjournals.molbev.a040454

Schindler C A, Schuhardt V T. 1964. Lysostaphin:A new bacteriolytic agent for the Staphylococcus. Proceedings of the National Academy of Sciences of the United States of America, 51(3):414-421, doi: 10.1073/pnas.51.3.414

Talbot V, Bianchi M. 1997. Bacterial proteolytic activity in sediments of the Subantarctic Indian Ocean sector. Deep Sea Research Part Ⅱ:Topical Studies in Oceanography, 44(5):1069-1084, doi: 10.1016/S0967-0645(96)00107-5

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, doi: 10.1093/molbev/msr121

Tsuboi S, Yamamura S, Imai A, et al. 2014. Linking temporal changes in bacterial community structures with the detection and phylogenetic analysis of neutral metalloprotease genes in the sediments of a hypereutrophic lake. Microbes and Environments, 29(3):314-321, doi: 10.1264/jsme2.me14064

Yan Bingqiang, Chen Xiulan, Hou Xiaoyan, et al. 2009. Molecular analysis of the gene encoding a cold-adapted halophilic subtilase from deep-sea psychrotolerant bacterium Pseudoalteromonas sp. SM9913:cloning, expression, characterization and function analysis of the C-terminal PPC domains. Extremophiles, 13(4):725-733, doi: 10.1007/s00792-009-0263-1

Yang Xiangsheng, Chen Xinglin, Xu Xianzhong, et al. 2011. Cold-adaptive alkaline protease from the psychrophilic Planomicrobium sp. 547:enzyme characterization and gene cloning. Advances in Polar Science, 22(1):49-54, doi: 10.3724/SP.J.1085.2011.00049

Yang Jian, Li Jie, Mai Zhimao, et al. 2013. Purification, characterization, and gene cloning of a cold-adapted thermolysin-like protease from Halobacillus sp. SCSIO 20089. Journal of Bioscience and Bioengineering, 115(6):628-632, doi: 10.1016/j.jbiosc.2012.12.013

Zhang Xiying, Han Xiaoxu, Chen Xiulan, et al. 2015. Diversity of cultivable protease-producing bacteria in sediments of Jiaozhou Bay, China. Frontiers in Microbiology, 6:1021, doi: 10.3389/fmicb.2015.01021

Zhao Huilin, Chen Xiulan, Xie Binbin, et al. 2012. Elastolytic mechanism of a novel M23 metalloprotease pseudoalterin from deep-sea Pseudoalteromonas sp. CF6-2:cleaving not only glycyl bonds in the hydrophobic regions but also peptide bonds in the hydrophilic regions involved in cross-linking. Journal of Biological Chemistry, 287(47):39710-39720, doi: 10.1074/jbc.M112.405076

Zhao Guoyan, Chen Xiulan, Zhao Huilin, et al. 2008. Hydrolysis of insoluble collagen by deseasin MCP-01 from deep-sea Pseudoalteromonas sp. SM9913:collagenolytic characters, collagen-binding ability of C-terminal polycystic kidney disease domain, and implication for its novel role in deep-sea sedimentary particulate organic nitrogen degradation. Journal of Biological Chemistry, 283(52):36100-36107, doi: 10.1074/jbc.M804438200

Zhou Mingyang, Chen Xiulan, Zhao Huilin, et al. 2009. Diversity of both the cultivable protease-producing bacteria and their extracellular proteases in the sediments of the South China sea. Microbial Ecology, 58(3):582-590, doi: 10.1007/s00248-009-9506-z

Zhou Mingyang, Wang Guanglong, Li Dan, et al. 2013. Diversity of both the cultivable protease-producing bacteria and bacterial extracellular proteases in the coastal sediments of King George Island, Antarctica. PLoS One, 8(11):e79668, doi: 10.1371/journal.pone.0079668

Zimmerman A E, Martiny A C, Allison S D. 2013. Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. The ISME Journal, 7(6):1187-1199, doi: 10.1038/ismej.2012.176

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