Abstract
Extremophile bacteria have developed the metabolic machinery for living in extreme temperatures, pH, and high-salt content. Two novel bacterium strains Alicyclobacillus sp. PA1 and Alicyclobacillus sp. PA2, were isolated from crater lake El Chichon in Chiapas, Mexico. Phylogenetic tree analysis based on the 16SrRNA gene sequence revealed that the strain Alicyclobacillus sp. PA1 and Alicyclobacillus sp. PA2 were closely related to Alicyclobacillus species (98% identity and 94.73% identity, respectively). Both strains were Gram variable, and colonies were circular, smooth and creamy. Electron microscopy showed than Alicyclobacillus sp. PA1 has a daisy-like form and Alicyclobacillus sp. PA2 is a regular rod. Both strains can use diverse carbohydrates and triglycerides as carbon source and they also can use organic and inorganic nitrogen source. But, the two strains can grow without any carbon or nitrogen sources in the culture medium. Temperature, pH and nutrition condition affect bacterial growth. Maximum growth was produced at 65 °C for Alicyclobacillus sp. PA1 (0.732 DO600) at pH 3 and Alicyclobacillus sp. PA2 (0.725 DO600) at pH 5. Inducible extracellular extremozyme activities were determined for β–galactosidase (Alicyclobacillus sp. PA1: 88.07 ± 0.252 U/mg, Alicyclobacillus sp. PA2: 51.57 ± 0.308 U/mg), cellulose (Alicyclobacillus sp. PA1: 141.20 ± 0.585 U/mg, Alicyclobacillus sp. PA2: 51.57 ± 0.308 U/mg), lipase (Alicyclobacillus sp. PA1: 138.25 ± 0.600 U/mg, Alicyclobacillus sp. PA2: 175.75 ± 1.387 U/mg), xylanase (Alicyclobacillus sp. PA1: 174.72 ± 1.746 U/mg, Alicyclobacillus sp. PA2: 172.69 ± 0.855U/mg), and protease (Alicyclobacillus sp. PA1: 15.12 ± 0.121 U/mg, Alicyclobacillus sp. PA2: 15.33 ± 0.284 U/mg). These results provide new insights on extreme enzymatic production on Alicyclobacillus species.
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References
Akanbi TO, Agyei D, Saari N (2019) Food Enzymes From Extreme Environments: Sources and Bioprocessing. In Enzymes Food Biotechnology 1st ed. Elsevier, London, pp 795-816
Albuquerque L, Rainey FA, Chung AP, Sunna A, Nobre MF, Grote R, Antranikian G, Da Costa MS (2000) Alicyclobacillus hesperidum sp. nov. and a related genomic species from solfataric soils of Sao Miguel in the Azores. Int J Syst Evol Microbiol 50:451–457. https://doi.org/10.1099/00207713-50-2-451
Armienta MA, De la Cruz-Reyna S, Ramos S, Ceniceros N, Cruz O, Aguayo A, Arcega-Cabrera F (2014) Hydrogeochemical surveillance at El Chichón volcano crater lake, Chiapas, Mexico. J Volcanol Geothermal Res 285:118–128. https://doi.org/10.1016/j.jvolgeores.2014.08.011(Armientaetal.2014)
Arroyo FA, Siering PL, Hampton JS, McCartney A, Hurst MP, Wolfe GV, Wilson MS (2015) Isolation and characterization of novel iron-oxidizing autotrophic and mixotrophic bacteria from boiling springs lake, an oligotrophic. Acid Geotherm Habitat Geomicrobiol J 32:140–217. https://doi.org/10.1080/01490451.2014.935533
Bevilacqua A, Mischitelli M, Pietropaolo V, Ciuffreda E, Sinigaglia M, Corbo MR (2015) Genotypic and phenotypic heterogeneity in Alicyclobacillus acidoterrestris: a contribution to species characterization. PLoS ONE 10:1–17. https://doi.org/10.1371/journal.pone.0141228
Bhalla A, Bischoff KM, Sani RK (2015) Highly thermostable xylanase production from a thermophilic Geobacillus sp. strain WSUCF1 utilizing lignocellulosic biomass. Front Bioeng Biotechnol 3:1–8. https://doi.org/10.3389/fbioe.2015.00084
Bowers KJ, Mesbah NM, Wiegel J (2009) Biodiversity of poly-extremophilic Bacteria: does combining the extremes of high salt, alkaline pH and elevated temperature approach a physico-chemical boundary for life? Saline Syst 9:1–8. https://doi.org/10.1186/1746-1448-5-9
Burns RG (2010) How do microbial extracellular enzymes Locate and Degrade Natural and Synthetic Polymers in Soil. In Molecular Environmental Soil Science at the Interfaces in the Earth’s Critical Zone. Springer, Berlin, pp 294-297
Carevic M, Vukasinovic-Sekulic M, Grabavcic S, Stojanovic M, Mihailovic M, Dimitrijevic A, Besbradica D (2015) Optimization of β-galactosidase production from lactic bacteria. Chem Ind J 69:305–312. https://doi.org/10.2298/HEMIND140303044C
Ciuffreda E, Bevilacqua A, Sinigaglia M, Corbo M (2015) Alicyclobacillus spp.: new insights on ecology and preserving food quality through new approaches. Microorganisms 3:625–640. https://doi.org/10.3390/microorganisms3040625
Coker JA (2016) Extremophiles and biotechnology: current uses and prospects. F1000 Res 5:1–7. https://doi.org/10.12688/f1000research.7432.1
Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23. https://doi.org/10.1016/j.femsre.2004.06.005
Cowan DA, Ramond JB, Makhalanyane TP, De Maayer P (2015) Metagenomics of extreme environments. Curr Opin Microbiol 25:97–102. https://doi.org/10.1016/j.mib.2015.05.005
Dalmaso GZ, Ferreira D, Vermelho AB (2015) Marine extremophiles: a source of hydrolases for biotechnological applications. Mar Drugs 13:1925–1965. https://doi.org/10.3390/md13041925
De Cassia PJ, Paganini Marques N, Rodrigues A, Brito de Oliveira T, Boscolo M, Da Silva R, Gomes E, Bocchini Martins DA (2015) Thermophilic fungi as new sources for production of cellulases and xylanases with potential use in sugarcane bagasse saccharification. J Appl Microbiol 184:928–939. https://doi.org/10.1111/jam.12757
Dumorné K, Córdova DC, Astorga-Eló M, Renganathan P (2017) Extremozymes: a potential source for industrial applications. J Microbiol Biotechnol 27:649–659. https://doi.org/10.4014/jmb.1611.11006
Ellis JT, Magnuson TS (2012) Thermostable and Alkalistable Xylanases produced by the thermophilic bacterium Anoxybacillus flavithermus TWXYL3. ISRN Microbiol 2012:1–8. https://doi.org/10.5402/2012/517524
Espliego JME, Saiz VB, Torregrosa-Crespo J, Luque AV, Camacho Carrasco ML, Pire C, Bonete MJ, Martínez-Espinosa RM (2018) Extremophile enzymes and biotechnology. In Extremophiles 1st ed. CRC press, Boca Raton, Florida, pp 227-248
Ghose TK (1987) Measurement of cellulase activities. Pure Appl Chem 59:257–268. https://doi.org/10.1351/pac198759020257
Giovannelli D, Sievert SM, Hügler M, Markert S, Becher D, Schweder T, Vetriani C (2017) Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans. Elife 6:1–31. https://doi.org/10.7554/eLife.18990
Gomes D, Rodrigues AC, Domingues L, Gama M (2015) Cellulase recycling in biorefineries—is it possible? Appl Microbiol Biotechnol 99:4131–4143. https://doi.org/10.1007/s00253-015-6535-z
Goto K, Mochida K, Kato Y, Asahara M, Fujita R, An SY, Kasai H, Yokota A (2007) Proposal of six species of moderately thermophilic, acidophilic, endospore-forming bacteria: Alicyclobacillus contaminans sp. nov., Alicyclobacillus fastidiosus sp. nov., Alicyclobacillus kakegawensis sp. nov., Alicyclobacillus macrosporangiidus sp. nov. Int J Syst Evol Microbiol 57:1276–1285. https://doi.org/10.1099/ijs.0.64692-0
Gul-Guven R, Guven K, Poli A, Nicolaus B (2007) Purification and some properties of a β-galactosidase from the thermoacidophilic Alicyclobacillus acidocaldarius subsp. rittmannii isolated from Antarctica. Enzyme Microb Tech 40:1570–1577. https://doi.org/10.1016/j.enzmictec.2006.11.006
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hammond JB, Kruger NJ (2012) The Bradford method for protein quantitation. Method Mol Biol 3:25–32. https://doi.org/10.1385/0-89603-126-8:25
Hirata H, Fukuzawa T, Negoro S, Okada H (1986) Structure of a β-galactosidase gene of Bacillus stearothermophilus. J Bacteriol 166:722–727. https://doi.org/10.1128/jb.166.3.722-727.1986
Hu J, Arantes V, Pribowo A, Saddler JN (2013) The synergistic action of accessory enzymes enhances the hydrolytic potential of a “cellulase mixture” but is highly substrate specific. Biotechnol Biofuels. https://doi.org/10.1186/1754-6834-6-112
Ibrahim ASS, Al-Salamah AA, Elbadawi YB, El-Tayeb MA, Shebl ISS (2015) Production of extracellular alkaline protease by new halotolerant alkaliphilic Bacillus sp. NPST-AK15 isolated from hyper saline soda lakes. Electron J Biotechnol 18:236–243. https://doi.org/10.1016/j.ejbt.2015.04.001
Ishikawa K, Kataoka M, Yanamoto T, Nakabayashi M, Watanabe M, Ishihara S, Yamaguchi S (2015) Crystal structure of β-galactosidase from Bacillus circulans ATCC 31382 (BgaD) and the construction of the thermophilic mutants. FEBS J 282:2540–2552. https://doi.org/10.1111/febs.13298
Jones D (1981) Manual of methods for general bacteriology. J Clin Pathology. Society for Microbiology. Washington, D.C
Justice NB, Norman A, Brown CT, Singh A, Thomas BC, Banfield JF (2014) Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms. BMC Genomics. https://doi.org/10.1186/1471-2164-15-1107
Kang Q, Zhang D (2020) Principle and potential applications of the non-classical protein secretory pathway in bacteria. Appl Microbiol Biotechnol 104:953–956. https://doi.org/10.1007/s00253-019-10285-4
Kim IJ, Nam KH, Yun EJ, Kim S, Youn HJ, Lee HJ, Choi IG, Kim KH (2015) Optimization of synergism of a recombinant auxiliary activity 9 from Chaetomium globosum with cellulase in cellulose hydrolysis. Appl Microbiol Biotechnol 99:8537–8547. https://doi.org/10.1007/s00253-015-6592-3
Kumar S, Kikon K, Upadhyay A, Kanwar SS, Gupta R (2005) Production, purification, and characterization of lipase from thermophilic and alkaliphilic Bacillus coagulans BTS-3. Protein Express Purif 41:38–44. https://doi.org/10.1016/j.pep.2004.12.010
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kusube M, Sugihara A, Moriwaki Y, Ueoka T, Shimane Y, Minegishi H (2014) Alicyclobacillus cellulosilyticus sp. nov., a thermophilic, cellulolytic bacterium isolated from steamed Japanese cedar chips from a lumbermill. Int J Syst Evol Microbiol 64:2257–2263. https://doi.org/10.1099/ijs.0.061440-0
Lama L, Calandrelli V, Gambacorta A, Nicolaus B (2004) Purification and characterization of thermostable xylanase and β-xylosidase by the thermophilic bacterium Bacillus thermantarcticus. Res Microbiol 155:283–289. https://doi.org/10.1016/j.resmic.2004.02.001
Lee DW, Koh YS, Kim KJ, Kim DS, Suhartono MT, Pyun YR (1999) Isolation and characterization of a thermophilic lipase from Bacillus thermoleovorans ID-1. FEMS Microbiol Lett 179:393–400. https://doi.org/10.1016/S0378-1097(99)00440-1
Li X, Yu HY (2013) Halostable cellulase with organic solvent tolerance from Haloarcula sp. LLSG7 and its application in bioethanol fermentation using agricultural wastes. J Ind Microbiol Biotechnol 40:1357–1365. https://doi.org/10.1007/s10295-013-1340-0
Li Q, Yi L, Marek P, Iverson BL (2013) Commercial proteases: present and future. FEBS Lett 587:1155–1163. https://doi.org/10.1016/j.febslet.2012.12.019
Li Y, Sun L-L, Sun Y-Y, Cha QQ, Li CY, Zhao DL, Song XY, Wang M, McMinn A, Chen XL, Zhang YZ, Qin QL (2019) Extracellular enzyme activity and its implications for organic matter cycling in northern Chinese marginal seas. Front Microbiol 10:1–13. https://doi.org/10.3389/fmicb.2019.02137
Liang YL, Zhang Z, Wu M, Wu Y, Feng JX (2014) Isolation, screening, and identification of cellulolytic bacteria from natural reserves in the subtropical region of China and optimization of cellulase production by Paenibacillus terrae ME27-1. Biomed Res Int 2014:1–13. https://doi.org/10.1155/2014/512497
Liang J, Mazur F, Tang C, Ning X, Chandrawati R, Liang K (2019) Peptide-induced super-assembly of biocatalytic metal-organic frameworks for programmed enzyme cascades. Chem Sci 10:7852–7858. https://doi.org/10.1039/c9sc02021g
Littlechild JA (2015) Enzymes from extreme environments and their industrial applications. Front Bioeng Biotechnol 3:161–170. https://doi.org/10.3389/fbioe.2015.00161
Lopez-Bedogini G, Massello FL, Giaveno A, Rubén-Donati E, Urbieta MS (2019) A deeper look into the biodiversity of the extremely acidic Copahue volcano-Río Agrio System in Neuquén, Argentina. Microorganisms 8:1–14. https://doi.org/10.3390/microorganisms8010058
Martínez-Espinosa RM (2020) Microorganisms and their metabolic capabilities in the context of the biogeochemical nitrogen cycle at extreme environments. Int J Mol Sci. https://doi.org/10.3390/ijms21124228
Mavromatis K, Sikorski J, Lapidus A, Del Rio TG, Copeland A, Tice H, Cheng JF, Lucas S, Chen F, Nolan M, Bruce D, Goodwin L, Pitluck S, Ivanova N, Ovchinnikova G, Pati A, Chen A, Palaniappan K, Land M, Kyrpides NC (2010) Complete genome sequence of Alicyclobacillus acidocaldarius type strain (104-IA T). Stand Genomic Sci. https://doi.org/10.4056/sigs.591104
McClure PJ (2006) Spore-forming bacteria. In Food Spoilage Microorganisms. Woodhead Publishing, Sawron, Reino Unido, pp 579-623
Méndez-García C, Peláez AI, Mesa V, Sánchez J, Golyshina OV, Ferrer M (2015) Microbial diversity and metabolic networks in acid mine drainage habitats. Front Microbiol 6:1–17. https://doi.org/10.3389/fmicb.2015.00475
Merino N, Aronson HS, Bojanova DP, Feyhl-Buska J, Wong ML, Zhang S, Giovannelli D (2019) Living at the extremes: extremophiles and the limits of life in a planetary context. Front Microbiol 10:780–805. https://doi.org/10.3389/fmicb.2019.00780
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Morana A, Esposito A, Maurelli L, Ruggiero G, Ionata E, Rossi M, Cara F (2008) A novel thermoacidophilic cellulase from Alicyclobacillus acidocaldarius. Protein Pept Lett 15:1017–1021. https://doi.org/10.2174/092986608785849209
Oliart-Ros R, Manresa-Presas Á, Sánchez-Otero G (2016) Utilization of microorganisms from extreme environments and their products in biotechnological development. Ciencia UAT 2:79–85
Pakarinen A, Haven MØ, Djajadi DT, Várnai A, Puranen T, Viikari L (2014) Cellulases without carbohydrate-binding modules in high consistency ethanol production process. Biotechnol Biofuels 7:27–38. https://doi.org/10.1186/1754-6834-7-27
Pant G, Prakash A, Pavani JVP, Bera S, Deviram GVNS, Kumar A, Panchpuri M, Prasuna RG (2015) Production, optimization and partial purification of protease from Bacillus subtilis. J Taibah Univ Sci 9:50–55. https://doi.org/10.1016/j.jtusci.2014.04.010
Pawlak-Szukalska A, Wanarska M, Popinigis AT, Kur J (2014) A novel cold-active β-d-galactosidase with transglycosylation activity from the Antarctic Arthrobacter sp. 32cB—gene cloning, purification and characterization. Process Biochem 49:2122–2133. https://doi.org/10.1016/j.procbio.2014.09.018
Pornpukdeewattana S, Jindaprasert A, Massa S (2019) Alicyclobacillus spoilage and control: a review. Crit Rev Food Sci 60:108–122. https://doi.org/10.1080/10408398.2018.1516190
Rampelotto PH (2013) Extremophiles and extreme environments. Life Sci 3:482–485. https://doi.org/10.3390/life3030482
Raval VH, Purohit MK, Singh SP (2013) Diversity, population dynamics and biocatalytic potential of cultivable and non-cultivable bacterial communities of the saline ecosystems. In Marine Enzymes for Biocatalysis 1st ed. Woodhead Publishing, Sawron, Reino Unido, pp 165-189
Remans T, Thijs S, Truyens S, Weyens N, Schellingen K, Keunen E, Gielen H, Cuypers A, Vangronsveld J (2012) Understanding the development of roots exposed to contaminants and the potential of plant-associated bacteria for optimization of growth. Ann Bot 110:239–252. https://doi.org/10.1093/aob/mcs105
Rhee JK, Ahn DG, Kim YG, Oh JW (2005) New thermophilic and thermostable esterase with sequence similarity to the hormone-sensitive lipase family, cloned from a metagenomic library. Appl Environ Microbiol 71:817–825. https://doi.org/10.1128/AEM.71.2.817-825.2005
Rincón-Molina CI, Hernández-García JA, Rincón-Rosales R, Gutiérrez-Miceli FA, Ramírez-Villanueva DA, González-Terreros E, Peña-Ocaña BA, Palomeque-Domínguez H, Dendooven L, Ruíz-Valdiviezo VM (2019) Structures and diversity of the bacterial communities in the acid and thermophilic cráter lake of the Volcano “El Chichón”, México. Geomicrobiol J 37:1–13. https://doi.org/10.1080/01490451.2018.1509158
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Salameh MA, Wiegel J (2007) Purification and characterization of two highly thermophilic alkaline lipases from Thermosyntropha lipolytica. Appl Environ Microbiol 73:7725–7731. https://doi.org/10.1128/AEM.01509-07
Schröder C, Burkhardt C, Antranikian G (2020) What we learn from extremophiles. ChemTexts 6:8–14. https://doi.org/10.1007/s40828-020-0103-6
Sharma A, Parashar D, Satyanarayana T (2016) Chapter 7 Acidophilic Microbes: Biology and Applications. In: Biotechnology of Extremophiles: Advances and Challenges 1st ed. Springer, Switzerland, pp 215-241
Shrestha N, Chilkoor G, Vemuri B, Rathinam N, Sani RK, Gadhamshetty V (2018) Extremophiles for microbial-electrochemistry applications: a critical review. Bioresour Technol 255:318–330. https://doi.org/10.1016/j.biortech.2018.01.151
Simbahan J, Drijber R, Blum P (2004) Alicyclobacillus vulcanalis sp. nov., a thermophilic acidophilic bacterium isolated from Coso Hot Springs, California, USA. Int J Syst Evol Microbiol 54:1703–1707. https://doi.org/10.1099/ijs.0.03012-0
Skirnisdottir S, Hreggvidsson GO, Holst O et al (2001) Isolation and characterization of a mixotrophic sulfur-oxidizing Thermus scotoductus. Extremophiles 5:45–51. https://doi.org/10.1007/s007920000172
Solís-Badillo M-R, Azaola-Espinosa G-N (2014) Identification of β-galactosidase, β-fructofuranosidase and glicosiltransferase enzymes from Cellulomonas flavigena when grown in several carbon sources. Rev Mex Ing Quím 13:583–593
Sorokin DY, Banciu HL, Muyzer G (2015) Functional microbiology of soda lakes. Curr Opin Microbiol 25:88–96. https://doi.org/10.1016/j.mib.2015.05.004
Tabssum F, Irfan M, Shakir HA, Qazi JI (2018) RSM based optimization of nutritional conditions for cellulase mediated Saccharification by Bacillus cereus. J Biol Eng 12:7–10. https://doi.org/10.1186/s13036-018-0097-4
Tsuruoka N, Isono Y, Shida O, Hemmi H, Nakayama T, Nishino T (2003) Alicyclobacillus sendaiensis sp. nov., a novel acidophilic, slightly thermophilic species isolated from soil in Sendai. Jpn Int J Syst Evol Microbiol 53:1080–1084. https://doi.org/10.1099/ijs.0.02409-0
Valdes J, Quatrini R, Hallberg K, Dopson M, Valenzuela PDT, Holmes DS (2009) Draft genome sequence of the extremely acidophilic bacterium Acidithiobacillus caldus ATCC 51756 reveals metabolic versatility in the genus Acidithiobacillus. J Bacteriol 191:5877–5878. https://doi.org/10.1128/JB.00843-09
Van den Burg B (2003) Extremophiles as a source for novel enzymes. Curr Opin Microbiol 6:213–218. https://doi.org/10.1016/S1369-5274(03)00060-2
Vorderwülbecke T, Kieslich K, Erdmann H (1992) Comparison of lipases by different assays. Enzyme Microb Tech 14:631–639. https://doi.org/10.1016/0141-0229(92)90038-P
Walia A, Mehta P, Guleria S, Shirkot CK (2015) Modification in the properties of paper by using cellulase-free xylanase produced from alkalophilic Cellulosimicrobium cellulans CKMX1 in biobleaching of wheat straw pulp. J Microbiol 61:671–681. https://doi.org/10.1139/cjm-2015-0178
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991
Wisotzkey JD, Jurtshuk P, Fox GE, Deinhard G, Poralla K (1992) Comparative sequence analyses on the 16S rRNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterrestris, and Bacillus cycloheptanicus and proposal for creation of a new genus, Alicyclobacillus gen. nov. Int J Syst Bacteriol 42:263–269. https://doi.org/10.1099/00207713-42-2-263
Wu C, Herold RA, Knoshaug EP, Wang B, Xiong W, Laurens LML (2019) Fluxomic analysis reveals central carbon metabolism adaptation for diazotroph Azotobacter vinelandii ammonium excretion. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-019-49717-6
Yahya A, Hallberg KB, Johnson DB (2008) Iron and carbon metabolism by a mineral-oxidizing Alicyclobacillus-like bacterium. Arch Microbiol 189:305–312. https://doi.org/10.1007/s00203-007-0319-5
Zhang X, She S, Dong W, Niu J, Xiao Y, Liang Y, Liu X, Zhang X, Fan F, Yin H (2016) Comparative genomics unravels metabolic differences at the species and/or strain level and extremely acidic environmental adaptation of ten bacteria belonging to the genus Acidithiobacillus. Syst Appl Microbiol 39:493–502. https://doi.org/10.1016/j.syapm.2016.08.007
Zhu D, Adebisi WA, Ahmad F, Sethupathy S, Danso B, Sun J (2020) Recent development of extremophilic bacteria and their application in biorefinery. Front Bioeng Biotechnol 1:1–18. https://doi.org/10.3389/fbioe.2020.00483
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The Ortiz-Cortés and Velázquez-Rios authors thank the Consejo Nacional de Ciencia y Tecnología (National Council of Science and Technology, México) for the scholarship granted.
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This work was supported by the Instituto de Ciencia, Tecnología e Innovación del Estado de Chiapas (Institute of Science, Technology and Innovation of Chiapas) project 2019–1016.
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Ortiz-Cortés, L., Ventura-Canseco, L., Abud-Archila, M. et al. Evaluation of temperature, pH and nutrient conditions in bacterial growth and extracellular hydrolytic activities of two Alicyclobacillus spp. strains. Arch Microbiol 203, 4557–4570 (2021). https://doi.org/10.1007/s00203-021-02332-4
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DOI: https://doi.org/10.1007/s00203-021-02332-4