Deciphering the role of dissolved oxygen and N-acetyl glucosamine in governing higher molecular weight hyaluronic acid synthesis in Streptococcus zooepidemicus cell factory.
Dissolved oxygen control strategy
Dual substrate kinetic model
Hyaluronic acid
N-acetyl glucosamine
Polydispersity index
S. zooepidemicus
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
Apr 2020
Apr 2020
Historique:
received:
21
08
2019
accepted:
06
02
2020
revised:
27
01
2020
pubmed:
23
2
2020
medline:
29
12
2020
entrez:
21
2
2020
Statut:
ppublish
Résumé
The present study is focused on systematic process and kinetic investigation of hyaluronic acid (HA) production strategy unraveling the role of dissolved oxygen (DO) and N-acetyl glucosamine (GlcNAc) towards the enhancement of HA titer and its molecular weight. Maintaining excess DO levels (10-40% DO) through DO-stat control and the substitution of GlcNAc at a range (5-20 g/L) with glucose (Glc) critically influenced HA production. DO-stat control strategy yielded a promising HA titer (2.4 g/L) at 40% DO concentration. Controlling DO level at 20% (DO-stat) was observed to be optimum resulting in a significant HA production (2.1 g/L) and its molecular weight ranging 0.98-1.45 MDa with a consistent polydispersity index (PDI) (1.57-1.69). Substitution of GlcNAc with Glc at different proportions explicitly addressed the metabolic trade-off between HA titer and its molecular weight. GlcNAc substitution positively influenced the molecular weight of HA. The highest HA molecular weight (2.53 MDa) of two-fold increase compared with glucose as sole carbon substrate and narrower PDI (1.35 ± 0.18) was achieved for the 10:20 (Glc:GlcNAc) proportion. A novice attempt on modeling the uptake of dual substrates (Glc and GlcNAc) by Streptococcus zooepidemicus for HA production was successfully accomplished using double Andrew's growth model and the kinetic parameters were estimated reliably.
Identifiants
pubmed: 32078020
doi: 10.1007/s00253-020-10445-x
pii: 10.1007/s00253-020-10445-x
doi:
Substances chimiques
Hyaluronic Acid
9004-61-9
Glucose
IY9XDZ35W2
Oxygen
S88TT14065
Acetylglucosamine
V956696549
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3349-3365Subventions
Organisme : Department of Biotechnology , Ministry of Science and Technology
ID : BT/PR5789/PID/6/680/2012
Références
Afzal M, Shafeeq S, Manzoor I, Henriques-Normak B, Kuipers OP (2016) N-acetyl glucosamine-mediated expression of nagA and nagB in Streptococcus pneumoniae. Front Cell Infect Microbial 6:158. https://doi.org/10.3389/fcimb.2016.00158
doi: 10.3389/fcimb.2016.00158
Amado IR, Vázquez JA, Pastrana L, Teixeira JA (2016) Cheese whey: a cost effective alternative for hyaluronic acid production by Streptococcus zooepidemicus. Food Chem 198:54–61. https://doi.org/10.1016/j.foodchem.2015.11.062
doi: 10.1016/j.foodchem.2015.11.062
pubmed: 26769504
Andre P (2004) Hyaluronic acid and its use as “rejuvenation” agent in cosmetic dermatology. SeminCutan Med Surg 23:218–222. https://doi.org/10.1016/j.sder.2004.09.002
doi: 10.1016/j.sder.2004.09.002
Armstrong DC, Johns MR (1997) Culture conditions affect the molecular weight properties of hyaluronic acid produced by Streptococcus zooepidemicus. Appl Environ Microbiol 63:2759–2764
doi: 10.1128/AEM.63.7.2759-2764.1997
Badle SS, Jayaraman G, Ramachandran KB (2014) Ratio of intracellular precursors concentrations and their flux influences hyaluronic acid molecular weight in Streptococcus zooepidemicus and recombinant Lactococcus lactis. Bioresour Technol 163:222–227. https://doi.org/10.1016/j.biortech.2014.04.027
doi: 10.1016/j.biortech.2014.04.027
pubmed: 24814248
Bapat PM, Bhartiya S, Venkatesh KV, Wangikar PP (2006) Structured kinetic model to represent the utilization of multiple substrates in complex media during rifamycin B fermentation. Biotechnol Bioeng 93:779–790. https://doi.org/10.1002/bit.20767
doi: 10.1002/bit.20767
pubmed: 16302259
Beyenal H, Chen SN, Lewandowski Z (2003) The double substrate growth kinetics of Pseudomonas aeruginosa. Enzyme Microb Technol 32:92–98. https://doi.org/10.1016/S0141-0229(02)00246-6
doi: 10.1016/S0141-0229(02)00246-6
Blank LM, Hugenholtz P, Nielsen LK (2008) Evolution of the hyaluronic acid synthesis (has) in Streptococcus zooepidemicus and other pathogenic Streptococci. J Mol Evol 67:13–22. https://doi.org/10.1007/s00239-008-9117-1
doi: 10.1007/s00239-008-9117-1
pubmed: 18551332
Chen WY, Marcellin E, Steen JA, Nielsen LK (2014) The role of hyaluronic acid precursor concentrations in molecular weight control in Streptococcus zooepidemicus. Mol Biotechnol 56:147–156. https://doi.org/10.1007/s12033-013-9690-4
doi: 10.1007/s12033-013-9690-4
pubmed: 23903961
Cheng F, Gong Q, Yu H, Stephanopoulus G (2016) High-titer biosynthesis of hyaluronic acid by recombinant Corynebacterium glutamicum. Biotechnol J 11:574–584. https://doi.org/10.1002/biot.201500404
doi: 10.1002/biot.201500404
pubmed: 26709615
Cheng F, Luozhang S, Guo Z, Yu H, Stephanopoulus G (2017) Enhanced biosynthesis of hyaluronic acid using engineered Corynebacterium glutamicum via metabolic pathway regulation. Biotechnol J 12:1700191. https://doi.org/10.1002/biot.201700191
doi: 10.1002/biot.201700191
Cheng F, Yu H, Stephanopoulus G (2019) Engineering Corynebacterium glutamicumfor high-titer biosynthesis of hyaluronic acid. Metab Eng 55:276–289. https://doi.org/10.1016/j.ymben.2019.07.003
doi: 10.1016/j.ymben.2019.07.003
pubmed: 31301358
DeAngelis PL, Jing W, Drake RR, Achyuthan AM (1998) Identification and molecular cloning of a unique hyaluronan synthase from Pasteurella multocida. J Biol Chem 273:8454–8458. https://doi.org/10.1074/jbc.273.14.8454
doi: 10.1074/jbc.273.14.8454
pubmed: 9525958
Don MM, Shoparwe NF (2010) Kinetics of hyaluronic acid production by Streptococcus zooepidemicus considering the effect of glucose. Biochem Eng J 49:95–103. https://doi.org/10.1016/j.bej.2009.12.001
doi: 10.1016/j.bej.2009.12.001
Ghodke RS, Kakati JP, Tadi SRR, Mohan N, Sivaprakasam S (2018) Kinetic modeling of hyaluronic acid production in palmyra palm (Borassus flabellifer) based medium by Streptococcus zooepidemicus MTCC 3523. Biochem Eng J 137:284–293. https://doi.org/10.1016/j.bej.2018.06.011
doi: 10.1016/j.bej.2018.06.011
Göllner I, Voss W, von Hehn U, Kammerer S (2017) Ingestion of an oral hyaluronan solution improves skin hydration, wrinkle reduction, elasticity and skin roughness: results of a clinical study. J Evid Based Complementary Altern Med 22:816–823. https://doi.org/10.1177/2156587217743640
doi: 10.1177/2156587217743640
pubmed: 29228816
pmcid: 5871318
Hoffmann J, Altenbuchner J (2014) Hyaluronic acid production with: effect of media composition on yield and molecular weight. Journal of Applied Microbiology 117 (3):663-678
Huang WC, Chen SJ, Chen TL (2006) The role of dissolved oxygen and function of agitation in hyaluronic acid fermentation. Biochem Eng J 32:239–243. https://doi.org/10.1016/j.bej.2006.10.011
doi: 10.1016/j.bej.2006.10.011
Huerta-Ángeles G, Nešporová K, Ambrožová G, Kubala L, Velebný V (2018) An effective translation: the development of hyaluronan-based medical products from the physiochemical, and preclinical aspects. Front Bioeng Biotechnol 6:62. https://doi.org/10.3389/fbioe.2018.00062
doi: 10.3389/fbioe.2018.00062
pubmed: 29868577
pmcid: 5966713
Izawa N, Serata M, Sone T, Osama T, Ohtake H (2011) Hyaluronic acid production by recombinant Streptococcus thermophilus. J Biosci Bioeng 111:665–670. https://doi.org/10.1016/j.jbiosc.2011.02.005
doi: 10.1016/j.jbiosc.2011.02.005
pubmed: 21371932
Jagannath S, Ramachandran KB (2010) Influence of competing metabolic processes on the molecular weight of hyaluronic acid synthesized by Streptococcus zooepidemicus. Biochem Eng J 48:148–158. https://doi.org/10.1016/j.bej.2009.09.003
doi: 10.1016/j.bej.2009.09.003
Jeeva P, Shanmuga DS, Sundaram V, Jayaraman G (2019) Production of controlled molecular weight hyaluronic acid by glucostat strategy using recombinant Lactococcus lactis cultures. Appl Microbiol Biotechnol 103:4363–4375. https://doi.org/10.1007/s00523-019-09769-0
doi: 10.1007/s00523-019-09769-0
pubmed: 30968163
Jeong E, Shim YW, Kim HJ (2014) Metabolic engineering of Pichia pastoris for production of hyaluronic acid with high molecular weight. J Biotechnol 20:28–36. https://doi.org/10.1016/j.jbiotec.2014.05.018
doi: 10.1016/j.jbiotec.2014.05.018
Jia Y, Zhu J, Chen X, Tang D, Su D, Yao W, Gao X (2013) Metabolic engineering of Bacillus subtilis for the efficient synthesis of uniform hyaluronic acid with controlled molecular weights. BioresourTechnol 132:427–431. https://doi.org/10.1016/j.biortech.2012.12.150
doi: 10.1016/j.biortech.2012.12.150
Lam J, Truong NF, Segura T (2014) Design of cell-matrix interactions in hyaluronic acid hydrogel scaffolds. Acta Biomater 10:1571–1580. https://doi.org/10.1016/j.actbio.2013.07.025
doi: 10.1016/j.actbio.2013.07.025
pubmed: 23899481
Li L, Duan X, Fan Z, Chen L, Xing F, Xu Z, Chen Q, Xiang Z (2018) Mesenchymal stem cells in combination with hyaluronic acid for articular cartilage defects. Sci Rep 8:9900. https://doi.org/10.1038/s41598-018-27737-y
doi: 10.1038/s41598-018-27737-y
pubmed: 29967404
pmcid: 6028658
Liang-Jung C, Cheng-Kang L (2007a) Enhanced hyaluronic acid production in Bacilllus subtilis by coexpressing bacterial hemoglobin. Biotechnol Prog 23:1017–1022. https://doi.org/10.1021/bp070036w
Liang-Jung C, Cheng-Kang L (2007b) Hyaluronic acid production by recombinant Lactococcus lactis. Applied Microbiology and Biotechnology 77 (2):339-346
Liu L, Wang M, Du G, Chen J (2008) Enhanced hyaluronic acid production of Streptococcus zooepidemicus by an intermittent alkaline-stress strategy. Lett Appl Microbiol 46:383–388. https://doi.org/10.1111/j.1472-765X.2008.02325.x
doi: 10.1111/j.1472-765X.2008.02325.x
pubmed: 18221275
Liu L, Du G, Chen J, Wang M, Sun J (2009a) Microbial production of low molecular weight hyaluronic acid by adding hydrogen peroxide and ascorbate in batch culture of Streptococcus zooepidemicus. Bioresour Technol 100:362–367. https://doi.org/10.1016/j.biortech.2008.05.040
doi: 10.1016/j.biortech.2008.05.040
pubmed: 18619838
Liu L, Du G, Chen J, Wang M, Sun J (2009b) Comparative study on the influence of dissolved oxygen control approaches on the microbial hyaluronic acid production of Streptococcus zooepidemicus. Bioprocess BiosystEng 32:755–763. https://doi.org/10.1007/s00449-009-0300-6
doi: 10.1007/s00449-009-0300-6
Liu J, Wang Y, Li Z, Ren Y, Zhao Y, Zhao G (2018) Efficient production of high-molecular-weight hyaluronic acid with a two-stage fermentation. RSC Adv 63:36167–36171. https://doi.org/10.1039/c8ra07349j
doi: 10.1039/c8ra07349j
Mao Z, Chen RR (2007) Recombinant synthesis of hyaluronan by Agrobacterium sp. Biotechnol Prog 23:1038–1042. https://doi.org/10.1021/bp070113n
doi: 10.1021/bp070113n
pubmed: 17705506
Medvedeva EV, Grebenik EA, Gornostaeva SN, Telpuhov VI, Lychagin AV, Timashev PS, Chagin AS (2018) Repair of damaged articular cartilage: current approaches and future directions. Int J MolSci 19:2366. https://doi.org/10.3390/ijms19082366
doi: 10.3390/ijms19082366
Meyer K, Palmer JW (1934) The polysaccharide of vitreous humor. J BiolChem 107:629–634
Mohan N, Pavan SS, Achar A, Swaminathan N, Sivaprakasam S (2019) Calorespirometric investigation of Streptococcus zooepidemicus metabolism: thermodynamics of anabolic payload contribution by growth and hyaluronic acid synthesis. BiochemEng J 152:107367. https://doi.org/10.1016/j.bej.2019.107367
doi: 10.1016/j.bej.2019.107367
Moye ZD, Burne AR, Zeng L (2014) Uptake and metabolism of N-acetyl glucosamine and glucosamine by Streptococcus mutans. Appl Environ Microbiol 80:5063–5067. https://doi.org/10.1128/AEM.00820-14
doi: 10.1128/AEM.00820-14
Prasad SB, Jayaraman G, Ramachandran KB (2010) Hyaluronic acid production is enhanced by the additional co-expression of UDP-glucose pyrophosphorylase in Lactococcus lactis. Appl Microbiol Biotechnol 86:273–283. https://doi.org/10.1007/s00253-009-2293-0
doi: 10.1007/s00253-009-2293-0
pubmed: 19862515
Puvendran K, Jayaraman G (2019) Enhancement of acetyl-CoA by acetate co-utilization in recombinant Lactococcus lactis cultures enables the production of high molecular weight hyaluronic acid. Appl Microbiol Biotechnol 103:6989–7001. https://doi.org/10.1007/s00253-019-09987-6
doi: 10.1007/s00253-019-09987-6
pubmed: 31267232
Shah MV, Badle SS, Ramachandran KB (2013) Hyaluronic acid production and molecular weight improvement by redirection of carbon flux towards its biosynthesis pathway. Biochem Eng J 80:53–60. https://doi.org/10.1016/j.bej.2013.09.013
doi: 10.1016/j.bej.2013.09.013
Sheng J, Ling P, Wang F (2015) Constructing a recombinant hyaluronic acid biosynthesis operon and producing food-grade hyaluronic acid in Lactococcus lactis. J Ind Microbiol Biotechnol 42:197–206. https://doi.org/10.1007/s10295-014-1555-8
doi: 10.1007/s10295-014-1555-8
pubmed: 25447786
Shuler, Kargi (2002) Bioprocess engineering: basic concepts. Prentice Hall, Upper Saddle River
Siegman S, Truong NF, Segura T (2015) Encapsulation of PEGylated and low-molecular-weight PEI polyplexes in hyaluronic acid hydrogels reduces aggegration. Acta Biomater 28:45–54. https://doi.org/10.1016/j.actbio.2015.09.020
doi: 10.1016/j.actbio.2015.09.020
pubmed: 26391497
pmcid: 4648651
Tamer TM (2013) Hyaluronan and synovial joint: function, distribution and healing. InterdiscipToxicol 6:111–125. https://doi.org/10.2478/intox-2013-0019
doi: 10.2478/intox-2013-0019
Thomas EL, Pera KA (1983) Oxygen metabolism of Streptococcus mutans: uptake of oxygen and release of superoxide and hydrogen peroxide. J Bacteriol 154:1236–1244
doi: 10.1128/JB.154.3.1236-1244.1983
Vázquez JA, Pastrana L, Piñeiro C, Teixeira JA, Martin RIP, Amado IR (2015) Production of hyaluronic acid by Streptococcus zooepidemicus on protein substrates obtained from Scyliorhinus canicula discards. Mar Drugs 13:6537–6549. https://doi.org/10.3390/md13106537
doi: 10.3390/md13106537
pubmed: 26512678
pmcid: 4626705
Vincent HK, Percival SS, Conrad BP, Seay AN, Montero C, Vincent KR (2013) Hyaluronic acid (HA) viscosupplementation on synovial fluid inflammation in knee osteoarthritis: a pilot study. Open Orthop J 7:378–384. https://doi.org/10.2174/1874325001307010378
doi: 10.2174/1874325001307010378
pubmed: 24093052
pmcid: 3788189
Wendy YC, Esteban M, Jacky H, Lars KN (2009) Hyaluronan molecular weight is controlled by UDP-N-acetyl glucosamine concentration in Streptococccus zooepidemicus. J Biol Chem 284:18007–18014. https://doi.org/10.1074/jbc.M109.011999
doi: 10.1074/jbc.M109.011999
Westbrook AW, Ren X, Moo-Young M, Chou CP (2018) Application of hydrocarbon and perfluorocarbon oxygen vectors to enhance heterologous production of hyaluronic acid in engineered Bacillus subtilis. Biotechnol Bioeng 115:1239–1252. https://doi.org/10.1002/bit.26551
doi: 10.1002/bit.26551
pubmed: 29384194
Widner B, Behr R, von Dollen S, Tang M, Heu T, Sloma A, Sternberg D, De Angelis PL, Weigel PH, Brown S (2005) Hyaluronic acid production in Bacillus subtilis. Appl Environ Microbiol 71:3747–3752. https://doi.org/10.1128/AEM.71.7.3747
doi: 10.1128/AEM.71.7.3747
pubmed: 16000785
pmcid: 1168996
Xu Z, Xujie D, WenSong T (2010) Mechanism for the effect of agitation on the molecular weight of hyaluronic acid produced by Streptococcus zooepidemicus. Food Chem 119:1643–1646. https://doi.org/10.1016/j.foodchem.2009.09.014
doi: 10.1016/j.foodchem.2009.09.014
Yu H, Stephanopoulus G (2008) Metabolic engineering of Escherichia coli for biosynthesis of hyaluronic acid. Metab Eng 10:24–32. https://doi.org/10.1016/j.ymben.2007.09.001
doi: 10.1016/j.ymben.2007.09.001
pubmed: 17959405
Zeng L, Burne AR (2015) NagR differentially regulates the expression of the glmS and nagAB genes required for amino sugar metabolism by Streptococcus mutans. J Bacteriol 197:3533–3544. https://doi.org/10.1128/JB.00606-15
doi: 10.1128/JB.00606-15
pubmed: 26324448
pmcid: 4621086