On the succinic acid production from xylose by growing and resting cells of Actinobacillus succinogenes: a comparison

  1. Escanciano, Itziar A.
  2. Ladero, Miguel
  3. Santos, Victoria E.
Revista:
Biomass Conversion and Biorefinery

ISSN: 2190-6815 2190-6823

Año de publicación: 2022

Volumen: 14

Número: 5

Páginas: 6533-6546

Tipo: Artículo

DOI: 10.1007/S13399-022-02943-X GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Biomass Conversion and Biorefinery

Resumen

Succinic acid is a key platform chemical in modern biochemical manufacturing. Optimization of the production of succinic acid production in terms of product titers and economy of resources is of vital importance. In this work, we have studied the succinic acid production by using both produced using growing and resting cells of Actinobacillus succinogenes. First, the process catalyzed by resting cells was enabled by the development of a two-step inoculum strategy which was crucial for the bacterial adaptation to the carbon source. The process was performed in the absence of nitrogen source, disabling cell duplication, and restricting endogenous respiration. While the product yields were almost identical when using growing cells (0.44 g‧g−1) and cells in resting state (0.43 g‧g−1); very interestingly, the by-product formation was dramatically reduced when operating with resting cells. Next, the format of resting cells was studied; biofilms were found to be more active than cells in suspension, in terms of specific activity, but the lower cellular concentration in biofilms affected negatively the acid final titers. Finally, a complete and simplified kinetic model was proposed and successfully fitted to the relevant retrieved data of biomass, substrate, products, and by-products both in production with growing and resting cells. These results pave the way for the optimization of succinic acid production processes with reduced nitrogen source consumption, promoting a higher selectivity to the target acid, which facilitates the subsequent downstream separation operations

Información de financiación

Financiadores

Referencias bibliográficas

  • Esteban J, Yustos P, Ladero M (2018) Catalytic processes from biomass-derived hexoses and pentoses: A recent literature overview. Catalysts 8:1–39. https://doi.org/10.3390/catal8120637
  • Alexandri M, Schneider R, Papapostolou H et al (2019) Restructuring the conventional sugar beet industry into a novel biorefinery: fractionation and bioconversion of sugar beet pulp into succinic acid and value-added coproducts. ACS Sustain Chem Eng 7:6569–6579. https://doi.org/10.1021/acssuschemeng.8b04874
  • Garcia-Ochoa F, Vergara P, Wojtusik M et al (2021) Multi-feedstock lignocellulosic biorefineries based on biological processes: An overview. Ind Crops Prod 172:114062. https://doi.org/10.1016/j.indcrop.2021.114062
  • Bhatia SK, Jagtap SS, Bedekar AA et al (2020) Recent developments in pretreatment technologies on lignocellulosic biomass: effect of key parameters, technological improvements, and challenges. Biores Technol 300:122724. https://doi.org/10.1016/j.biortech.2019.122724
  • Haldar D, Purkait MK (2021) A review on the environment-friendly emerging techniques for pretreatment of lignocellulosic biomass: mechanistic insight and advancements. Chemosphere 264:128523. https://doi.org/10.1016/j.chemosphere.2020.128523
  • Bradfield MFA, Nicol W (2016) Continuous succinic acid production from xylose by Actinobacillus succinogenes. Bioprocess Biosyst Eng 39:233–244. https://doi.org/10.1007/s00449-015-1507-3
  • Jagtap SS, Rao CV (2018) Microbial conversion of xylose into useful bioproducts. Appl Microbiol Biotechnol 102:9015–9036. https://doi.org/10.1007/s00253-018-9294-9
  • Lu J, Li J, Gao H et al (2021) Recent progress on bio-succinic acid production from lignocellulosic biomass. World J Microbiol Biotechnol 37:1–8. https://doi.org/10.1007/s11274-020-02979-z
  • Stylianou E, Pateraki C, Ladakis D et al (2021) Optimization of fermentation medium for succinic acid production using Basfia succiniciproducens. Environ Technol Innov 24:101914. https://doi.org/10.1016/j.eti.2021.101914
  • Yang Q, Wu M, Dai Z, et al (2019) Comprehensive investigation of succinic acid production by Actinobacillus succinogenes: a promising native succinic acid producer. Biofuels Bioprod Biorefin 1–15. https://doi.org/10.1002/bbb.2058
  • Pateraki C, Patsalou M, Vlysidis A et al (2016) Actinobacillus succinogenes: advances on succinic acid production and prospects for development of integrated biorefineries. Biochem Eng J 112:285–303. https://doi.org/10.1016/j.bej.2016.04.005
  • Ahn JH, Seo H, Park W et al (2020) Enhanced succinic acid production by Mannheimia employing optimal malate dehydrogenase. Nat Commun 11(1):1–12. https://doi.org/10.1038/s41467-020-15839-z
  • Li C, Ong KL, Cui Z et al (2021) Promising advancement in fermentative succinic acid production by yeast hosts. J Hazard Mater 401:123414. https://doi.org/10.1016/j.jhazmat.2020.123414
  • Salma A, Djelal H, Abdallah R et al (2021) Well knowledge of the physiology of Actinobacillus succinogenes to improve succinic acid production. Appl Microbiol 1:304–328. https://doi.org/10.3390/applmicrobiol1020022
  • Amulya K, Kopperi H, Venkata Mohan S (2020) Tunable production of succinic acid at elevated pressures of CO2 in a high pressure gas fermentation reactor. Biores Technol 309:123327. https://doi.org/10.1016/j.biortech.2020.123327
  • Gonzales TA, Carvalho Silvello MA, de, Duarte ER, et al (2020) Optimization of anaerobic fermentation of Actinobacillus succinogenes for increase the succinic acid production. Biocatal Agric Biotechnol 27:101718. https://doi.org/10.1016/j.bcab.2020.101718
  • Ventrone M, Schiraldi C, Squillaci G et al (2020) Chestnut shells as waste material for succinic acid production from Actinobacillus succinogenes 130Z. Fermentation 6:105. https://doi.org/10.3390/fermentation6040105
  • de la Morena S, Wojtusik M, Santos VE, Garcia-Ochoa F (2020) Kinetic modeling of dihydroxyacetone production from glycerol by Gluconobacter oxydans ATCC 621 resting cells: Effect of fluid dynamics conditions. Catalysts 10(1):101. https://doi.org/10.3390/catal10010101
  • Ripoll V, Ladero M, Santos VE (2021) Kinetic modelling of 2,3-butanediol production by Raoultella terrigena CECT 4519 resting cells: effect of fluid dynamics conditions and initial glycerol concentration. Biochem Eng J 176:108185. https://doi.org/10.1016/j.bej.2021.108185
  • Salma A, Djelal H, Abdallah R et al (2021) Platform molecule from sustainable raw materials; case study succinic acid. Braz J Chem Eng 38:215–239. https://doi.org/10.1007/s43153-021-00103-8
  • de la Torre I, Ladero M, Santos VE (2020) D-lactic acid production from orange waste enzymatic hydrolysates with L. delbrueckii cells in growing and resting state. Ind Crops Prod 146:112176. https://doi.org/10.1016/j.indcrop.2020.112176
  • Alves PM, Carrondo MJT, Cruz PE (2008) Introduction to animal cell technology. Animal Cell Technology: From Biopharmaceuticals to Gene Therapy 1–12
  • Werf MJ Van Der, Guettler M V, Jain MK, Zeikus JG (2016) Environmental and physiological factors affecting the succinate product ratio during carbohydrate fermentation by Actinobacillus sp. 130Z. 2016. https://doi.org/10.1007/s002030050452
  • Mokwatlo SC, Nicol W (2017) Structure and cell viability analysis of Actinobacillus succinogenes biofilms as biocatalysts for succinic acid production. Biochem Eng J 128:134–140. https://doi.org/10.1016/j.bej.2017.09.013
  • Brink HG, Nicol W (2014) Succinic acid production with Actinobacillus succinogenes: rate and yield analysis of chemostat and biofilm cultures. Microb Cell Fact 13:111. https://doi.org/10.1186/s12934-014-0111-6
  • Acedos MG, De La Torre I, Santos VE, Garcia-Ochoa F (2019) Kinetic modeling of the isobutanol production from glucose using Shimwellia blattae (p424IbPSO) strain: effect of initial substrate concentration. Ind Eng Chem Res 58:1502–1512. https://doi.org/10.1021/acs.iecr.8b05121
  • Salvachúa D, Mohagheghi A, Smith H et al (2016) Succinic acid production on xylose-enriched biorefinery streams by Actinobacillus succinogenes in batch fermentation. Biotechnol Biofuels 9:28. https://doi.org/10.1186/s13068-016-0425-1
  • Zou W, Zhu L-W, Li H-M, Tang Y-J (2011) Significance of CO2 donor on the production of succinic acid by Actinobacillus succinogenes ATCC 55618. Microb Cell Fact 10:87. https://doi.org/10.1186/1475-2859-10-87
  • Song H, Kim TY, Choi B-K et al (2008) Development of chemically defined medium for Mannheimia succiniciproducens based on its genome sequence. Appl Microbiol Biotechnol 79:263–272. https://doi.org/10.1007/s00253-008-1425-2
  • Bumyut A, Champreda V, Singhakant C, Kanchanasuta S (2020) Effects of immobilization of Actinobacillus succinogenes on efficiency of bio-succinic acid production from glycerol. Biomass Convers Biorefin 12:643–654. https://doi.org/10.1007/s13399-020-01069-2
  • Patsalou M, Chrysargyris A, Tzortzakis N, Koutinas M (2020) A biorefinery for conversion of citrus peel waste into essential oils, pectin, fertilizer and succinic acid via different fermentation strategies. Waste Manage 113:469–477. https://doi.org/10.1016/j.wasman.2020.06.020
  • Oreoluwa Jokodola E, Narisetty V, Castro E et al (2022) Process optimisation for production and recovery of succinic acid using xylose-rich hydrolysates by Actinobacillus succinogenes. Biores Technol 344:126224. https://doi.org/10.1016/j.biortech.2021.126224
  • Almqvist H, Pateraki C, Alexandri M et al (2016) Succinic acid production by Actinobacillus succinogenes from batch fermentation of mixed sugars. J Ind Microbiol Biotechnol 43:1117–1130. https://doi.org/10.1007/s10295-016-1787-x
  • Ferone M, Raganati F, Olivieri G et al (2017) Biosuccinic acid from lignocellulosic-based hexoses and pentoses by Actinobacillus succinogenes: characterization of the conversion process. Appl Biochem Biotechnol 183:1465–1477. https://doi.org/10.1007/s12010-017-2514-4
  • Bradfield MFA, Nicol W (2014) Continuous succinic acid production by Actinobacillus succinogenes in a biofilm reactor: steady-state metabolic flux variation. Biochem Eng J 85:1–7. https://doi.org/10.1016/j.bej.2014.01.009
  • Xi YL, Chen KQ, Dai WY et al (2013) Succinic acid production by Actinobacillus succinogenes NJ113 using corn steep liquor powder as nitrogen source. Biores Technol 136:775–779. https://doi.org/10.1016/j.biortech.2013.03.107
  • Mokwatlo SC, Brink HG, Nicol W (2020) Effect of shear on morphology, viability and metabolic activity of succinic acid-producing Actinobacillus succinogenes biofilms. Bioprocess Biosyst Eng 43:1253–1263. https://doi.org/10.1007/s00449-020-02322-8
  • Mokwatlo SC, Nicol W, Brink HG (2021) Internal mass transfer considerations in biofilms of succinic acid producing Actinobacillus succinogenes. Chem Eng J 407:127220. https://doi.org/10.1016/j.cej.2020.127220
  • Li Q, Wang D, Wu Y et al (2010) Kinetic evaluation of products inhibition to succinic acid producers Escherichia coli NZN111, AFP111, BL21, and Actinobacillus succinogenes 130ZT. J Microbiol 48:290–296. https://doi.org/10.1007/s12275-010-9262-2
  • Corona-González RI, Bories A, González-Álvarez V, Pelayo-Ortiz C (2008) Kinetic study of succinic acid production by Actinobacillus succinogenes ZT-130. Process Biochem 43:1047–1053. https://doi.org/10.1016/j.procbio.2008.05.011
  • Sadhukhan S, Villa R, Sarkar U (2016) Microbial production of succinic acid using crude and purified glycerol from a Crotalaria juncea based biorefinery. Biotechnol Rep 10:84–93. https://doi.org/10.1016/j.btre.2016.03.008
  • Cimini D, Zaccariello L, D’Ambrosio S et al (2019) Improved production of succinic acid from Basfia succiniciproducens growing on A. donax and process evaluation through material flow analysis. Biotechnol Biofuels 12:22. https://doi.org/10.1186/s13068-019-1362-6
  • Luthfi AAI, Jahim JM, Harun S et al (2018) Kinetics of the bioproduction of succinic acid by Actinobacillus succinogenes from oil palm lignocellulosic hydrolysate in a bioreactor. BioResources 13:8279–8294. https://doi.org/10.15376/biores.13.4.8279-8294
  • Ferone M, Raganati F, Olivieri G et al (2019) Continuous succinic acid fermentation by Actinobacillus succinogenes: assessment of growth and succinic acid production kinetics. Appl Biochem Biotechnol 187:782–799. https://doi.org/10.1007/s12010-018-2846-8
  • Lin SKC, Du C, Koutinas A et al (2008) Substrate and product inhibition kinetics in succinic acid production by Actinobacillus succinogenes. Biochem Eng J 41:128–135. https://doi.org/10.1016/j.bej.2008.03.013
  • Pateraki C, Almqvist H, Ladakis D et al (2016) Modelling succinic acid fermentation using a xylose based substrate. Biochem Eng J 114:26–41. https://doi.org/10.1016/j.bej.2016.06.011
  • Vlysidis A, Binns M, Webb C, Theodoropoulos C (2011) Glycerol utilisation for the production of chemicals: conversion to succinic acid, a combined experimental and computational study. Biochem Eng J 58–59:1–11. https://doi.org/10.1016/j.bej.2011.07.004
  • de la Torre I, Acedos MG, Ladero M, Santos VE (2019) On the use of resting L. delbrueckii spp. delbrueckii cells for D-lactic acid production from orange peel wastes hydrolysates. Biochem Eng J 145:162–169. https://doi.org/10.1016/j.bej.2019.02.012