Abstract
To date, the genus Parvularcula consists of 6 species and no potential application of this genus was reported. Current study presents the genome sequence of Parvularcula flava strain NH6-79 T and its cellulolytic enzyme analysis. The assembled draft genome of strain NH6-79 T consists of 9 contigs and 7 scaffolds with 3.68 Mbp in size and GC content of 59.87%. From a total of 3,465 genes predicted, 96 of them are annotated as glycoside hydrolases (GHs). Within these GHs, 20 encoded genes are related to cellulosic biomass degradation, including 12 endoglucanases (5 GH10, 4 GH5, and 3 GH51), 2 exoglucanases (GH9) and 6 β-glucosidases (GH3). In addition, highest relative enzyme activities (endoglucanase, exoglucanase, and β-glucosidase) were observed at 27th hour when the strain was cultured in the carboxymethyl cellulose/Avicel®-containing medium for 45 h. The combination of genome analysis with experimental studies indicated the ability of strain NH6-79 T to produce extracellular endoglucanase, exoglucanase, and β-glucosidase. These findings suggest the potential of Parvularcula flava strain NH6-79 T in cellulose-containing biomass degradation and that the strain could be used in cellulosic biorefining process.
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References
Agrawal R, Verma AK, Satlewal A (2016) Application of nanoparticle-immobilized thermostable β-glucosidase for improving the sugarcane juice properties. Innov Food Sci Technol. https://doi.org/10.1016/j.ifset.2015.11.024
Almagro Armenteros J, Tsirigos KD (2019) SignalP 50 improves signal peptide predictions using deep neural networks. Nat Biotechnol 23:95
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol. https://doi.org/10.1016/S0022-2836(05)80360-2
Annamalai N, Rajeswari MV, Elayaraja S, Balasubramanian T (2013) Thermostable, haloalkaline cellulase from Bacillus halodurans CAS 1 by conversion of lignocellulosic wastes. Carbohyd Polym. https://doi.org/10.1016/j.carbpol.2013.01.066
Arun AB, Chen WM, Lai WA, Chou JH, Rekha PD, Shen FT, Young CC (2009) Parvularcula lutaonensis sp. nov., a moderately thermotolerant marine bacterium isolated from a coastal hot spring. Intern J Syst Microbiol 30:589–608
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. https://doi.org/10.1089/cmb.2012.0021
Beygmoradi A, Homaei A (2017) Marine microbes as a valuable resource for brand new industrial biocatalysts. Biocatal Agric Biotechnol. https://doi.org/10.1016/j.bcab.2017.06.013
Bhatnagar I, Kim SK (2010) Immense essence of excellence: Marine microbial bioactive compounds. Marine Drugs. https://doi.org/10.3390/md8102673
Biswas K, Paul D, Sinha SN (2016) Marine bacteria: a potential tool for antibacterial activity. J Appl Environ Microbiol 4:25–29
Borodovsky M, Lomsadze A (2014) Gene identification in prokaryotic genomes, phages, metagenomes, and EST sequences with GeneMarkS suite. Curr Microbiol. https://doi.org/10.1002/9780471729259.mc01e07s32
Castrejón-Godínez ML, Ortiz-Hernández ML, Salazar E, Encarnación S, Mussali-Galante P, Tovar-Sánchez E, Rodríguez A (2019) Transcriptional analysis reveals the metabolic state of Burkholderia zhejiangensis CEIB S4–3 during methyl parathion degradation. PeerJ. https://doi.org/10.7717/peerj.6822
Chmelová D, Ondrejovič M (2019) Determination of enzymes produced by Ceripriopsis subvermispora during pretreatment of different biomass sources. Microbiol Biotechnol Food Sci 5:9
Cho JC, Giovannoni SJ (2003) Parvularcula bermudensis gen. nov., sp. Nov., a marine bacterium that forms a deep branch in the α-Proteobacteria. J Microbiol 2:64
Chow V, Shantharaj D, Guo Y (2015) Xylan utilization regulon in Xanthomonas citri pv citri Strain Gene expression and utilization of oligoxylosides. Appl Environ Microbiol 2:9
Cortes-Tolalpa L, Salles JF, van Elsas JD (2017) Bacterial synergism in lignocellulose biomass degradation - complementary roles of degraders as influenced by complexity of the carbon source. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01628
Fatokun EN, Nwodo UU, Olaniran AO, Okoh AI (2017) Optimization of process conditions for the production of holocellulase by a Bacillus species isolated from Nahoon beach sediments. Am J Biochem Biotechnol. https://doi.org/10.3844/ajbbsp.2017.70.80
Finn RD, Attwood TK, Babbitt PC, Bateman A, Bork P, Bridge AJ, Mitchell AL (2017) InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw1107
Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol. https://doi.org/10.1016/S0959-440X(97)80072-3
Hu J, Gourlay K, Arantes V, Van Dyk JS, Pribowo A, Saddler JN (2015) The accessible cellulose surface influences cellulase synergism during the hydrolysis of lignocellulosic substrates. Chemsuschem. https://doi.org/10.1002/cssc.201403335
Hussain AA, Abdel-Salam MS, Abo-Ghalia HH, Hegazy WK, Hafez SS (2017) Optimization and molecular identification of novel cellulose degrading bacteria isolated from Egyptian environment. J Genetic Biotechnol. https://doi.org/10.1016/j.jgeb.2017.02.007
Lam MQ, Oates NC, Thevarajoo S, Tokiman L, Goh KM, McQueen-Mason SJ, Chong CS (2020) Genomic analysis of a lignocellulose degrading strain from the underexplored genus Meridianimaribacter. Genomics. https://doi.org/10.1016/j.ygeno.2019.06.011
Li S, Tang K, Liu K, Yu CP, Jiao N (2014) Parvularcula oceanus sp. Nov., isolated from deep-sea water of the Southeastern Pacific Ocean. Antonie van Leeuwenhoek, Intern J Molecular Microbiol 2:293–567
Liew KJ, Teo SC, Shamsir MS, Sani RK, Chong CS, Chan KG, Goh KM (2018) Complete genome sequence of Rhodothermaceae bacterium RA with cellulolytic and xylanolytic activities. Biotech 3:64–147
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. https://doi.org/10.1093/nar/gkt1178
Menendez E, Garcia-Fraile P, Rivas R (2015) Biotechnological applications of bacterial cellulases. AIMS Bioengin. https://doi.org/10.3934/bioeng.2015.3.163
Mewis K, Lenfant N, Lombard V, Henrissat B (2016) Dividing the large glycoside hydrolase family 43 into subfamilies: A motivation for detailed enzyme characterization. Appl Environ Microbiol. https://doi.org/10.1128/AEM.03453-15
Miller GL (1959) Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal Chem. https://doi.org/10.1021/ac60147a030
Muñoz C, Hidalgo C, Zapata M, Jeison D, Riquelme C, Rivas M (2014) Use of cellulolytic marine bacteria for enzymatic pretreatment in microalgal biogas production. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00827-14
Nakatani Y, Cutfield SM, Cowieson NP, Cutfield JF (2012) Structure and activity of exo-1,3/1,4-β-glucanase from marine bacterium Pseudoalteromonas sp BB1 showing a novel C-terminal domain. FEBS J 1:12–64
Pozzo T, Pasten JL, Karlsson EN, Logan DT (2010) Structural and functional analyses of β-Glucosidase 3B from Thermotoga neapolitana: A Thermostable three-domain representative of Glycoside hydrolase 3. J Mol Biol. https://doi.org/10.1016/j.jmb.2010.01.072
Rolfe MD, Rice CJ, Lucchini S, Pin C, Thompson A, Cameron ADS, Hinton JCD (2012) Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. J Bacteriol. https://doi.org/10.1128/JB.06112-11
Selvaratnam C, Thevarajoo S, Ee R, Chan KG, Bennett JP, Goh KM, Chong CS (2016) Genome sequence of Roseivirga sp strain D-25 and its potential applications from the genomic aspect. Marine Genomics 23:91
Shulami S, Shenker O, Langut Y, Lavid N, Gat O, Zaide G, Shoham Y (2014) Multiple regulatory mechanisms control the expression of the Geobacillus stearothermophilus gene for extracellular xylanase. J Biol Chem. https://doi.org/10.1074/jbc.M114.592873
Sun LL, Dang YR, Li Y, Qin QL, Su HN, Li PY, Zhang XY (2019) Parvularcula marina sp. nov., isolated from surface water of the South China Sea, and emended description of the genus Parvularcula. Intern J Syst Evolut Microbiol 95:246–743
Tatusova T, Dicuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw569
Thevarajoo S, Selvaratnam C, Chan KG, Goh KM, Chong CS (3516T) Draft genome sequence of Vitellibacter vladivostokensis KMM 3516T: a protease-producing bacterium. Marine Genomics. https://doi.org/10.1016/j.margen.2015.04.009
Trivedi N, Reddy CRK, Lali AM (2016) Marine microbes as a potential source of cellulolytic enzymes. Adv Food Nutr Res. https://doi.org/10.1016/bs.afnr.2016.07.002
Waghmare PR, Patil SM, Jadhav SL, Jeon BH, Govindwar SP (2018) Utilization of agricultural waste biomass by cellulolytic isolate Enterobacter sp SUK-Bio. Agr Nat Res 12:74–95. https://doi.org/10.1016/j.anres.2018.10.019
Wood TM, Bhat KM (1988) Methods for measuring cellulase activities. Methods Enzymol. https://doi.org/10.1016/0076-6879(88)60109-1
Wu S, Zhu Z, Fu L, Niu B, Li W (2011) WebMGA: A customizable web server for fast metagenomic sequence analysis. BMC Genomics. https://doi.org/10.1186/1471-2164-12-444
Yu Z, Lai Q, Li G, Shao Z (2013) Parvularcula dongshanensis sp. nov., isolated from soft coral. Intern J Syst Microbiol 687:9–47. https://doi.org/10.1099/ijs.0.044313-0
Zakaria MR, Lam MQ, Chen SJ, Abdul Karim MH, Tokiman L, Yahya A, Chong CS (2020) Genome sequence data of Mangrovimonas sp strain CR14 isolated from mangrove forest at Tanjung Piai National Park Malaysia. Data Brief 23:72. https://doi.org/10.1016/j.dib.2020.105658
Zhang T, Zhu J, Wei S, Luo Q, Li L, Li S, Zhou R (2016a) The roles of RelA/(p)ppGpp in glucose-starvation induced adaptive response in the zoonotic Streptococcus suis. Scientific Rep. https://doi.org/10.1038/srep27169
Zhang XQ, Wu YH, Zhou X, Zhang X, Xu XW, Wu M (2016b) Parvularcula flava sp nov, an Alphaproteobacterium isolated from surface seawater of the South China Sea. Intern J Syst Microbiol 76:94
Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Yin Y (2018) DbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. https://doi.org/10.1093/nar/gky418
Acknowledgement
This work was supported by Fundamental Research Grant Scheme (FRGS) from the Ministry of Education Malaysia with project number 5F196. Mohamad Hamizan Abdul Karim thanks the National Postgraduate Fund Program of Universiti Teknologi Malaysia for scholarship support. Ming Quan Lam is grateful to Khazanah Watan Postgraduate (PhD) scholarship (scholar ID: 40852) from Yayasan Khazanah. Sye Jinn Chen thanks the Zamalah scholarship from Universiti Teknologi Malaysia.
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Mohamad Hamizan Abdul Karim carried out the experiment, analyzed the data and drafted the manuscript. Ming Quan Lam designed the experiment, assisted in bioinformatics analyses and provided the expertise. Sye Jinn Chen assisted in performing the experiments and provided the expertise. Chun Shiong Chong conceived of the presented idea, designed the experiment and provided knowledge. Adibah Yahya, Shafinaz Shahir and Mohd Shahir Shamsir provided the expertise. All authors read, edited, justified, and approved the final manuscript.
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Abdul Karim, M.H., Lam, M.Q., Chen, S.J. et al. Draft genome sequence of Parvularcula flava strain NH6-79 T, revealing its role as a cellulolytic enzymes producer. Arch Microbiol 202, 2591–2597 (2020). https://doi.org/10.1007/s00203-020-01967-z
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DOI: https://doi.org/10.1007/s00203-020-01967-z