Abstract
This paper investigates the differences in some metabolites using Biolog FF Microplate™ system and the production of organic acids such as β-hydroxybutyric, p-hydroxyphenylacetic, and others. Another group of organic acids such as gluconic, oxalic and citric acid were studied during cultivation in a liquid medium. Four different Aspergillus niger (An) wild type strains were used as a model organism. Three strains, from the Banská Štiavnica – Šobov (An – Š), Pezinok (An – P) and Slovinky (An – Sl) localities were isolated from contaminated old mining areas with soil with ultra acidic to strong alkaline reactions. The fourth strain isolated from the Gabčíkovovo (An – G) locality was used for comparative purposes. According to the RAMP analysis, the strains are clustered into two groups, An – Š and An – P (similarity 82%), An – G and An – Sl (similarity 64%) which correlates with the pH values of the original environment. However, significant differences were found in metabolic processes in the reaction with a wide range of organic acids. In general, the reactions with D-lactic acid and D-malic acid correlate with the results of the RAMP analysis of fungal genotype similarities, the An – Š and An – P strains had an identical negative reaction, and an identical positive reaction was found in the An – Sl and An – G strains. During incubation the wild-type strains produced substantial amounts of gluconic acid, oxalic acid and small amounts of citric acid. The appearance and accumulation of organic acids was found to be highly pH dependent with the most active strain isolated from an ultra-acidic environment. The comparative strain differs entirely in the production of oxalic acid.
Similar content being viewed by others
References
Andersen MR, Lehmann L, Nielsen J (2009) Systemic analysis of the response of Aspergillus niger to ambient pH. Genome Biol 10:R47–R47. https://doi.org/10.1186/gb-2009-10-5-r47
Bercovitz A, Peleg Y, Battat E, Rokem JS, Goldberg I (1990) Localization of pyruvate carboxylase in organic acid-producing Aspergillus strains. Appl Environ Microbiol 56(6):1594–1597
Bochner BR (2009) Global phenotypic characterization of bacteria. FEMS Microbiol Rev 33(1):191–205. https://doi.org/10.1111/j.1574-6976.2008.00149.x
Carranza CS, Barberis CL, Chiacchiera SM, Magnoli CE (2017) Assesment of growth of Aspergillus spp. From agricultural soils in the presence of glyphosate. Rev Argen Microbiol 49(4):384–393. https://doi.org/10.1016/j.ram.2016.11.007
Cleland WW, Johnson MJ (1954) Tracer experiments on the mechanism of citric acid formation by Aspergillus niger. J Biol Chem 208:679–690. http://www.jbc.org/
Cochrane VW (1958) Physiology of fungi. Wiley, London
Dinh QT, Li Z, Tran TAT, Wang D, Liang D (2017) Role of organic acids on the bioavailability of selenium in soil: A review. Chemosphere 184:618–635. https://doi.org/10.1016/j.chemosphere.2017.06.034
Dutton MV, Evans CS (1996) Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can J Microbiol 42:881–895. https://doi.org/10.1139/m-114
Emiliani E, Bekes P (1964) Enzymatic oxalate decarboxylation in Aspergillus niger. Arch Biochem Biophys 105:488–493. https://doi.org/10.1016/0003-9861(64)90040-2
Eschenfeldt WH, Stols L, Rosenbaum H, Khambatta ZS, Quaite-Randall E, Wu S, Kilgore DC, Trent JD, Donnelly MI (2001) DNA from uncultured organisms as a source of 2,5-diketo-D-gluconic acid reductases. Appl Environ Microbiol 67(9):4206–4214. https://doi.org/10.1128/aem.67.9.4206-4216.2001
Gadd GM (1999) Fungal production of citric and oxalic acid: Importance in metal speciation, physiology and biogeochemical processes. Adv Microb Physiol 41:47–92. https://doi.org/10.1016/s0065-2911(08)60165-4
Gadd GM, Bahri-Esfahani J, Li Q, Rhee YJ, Wei Z, Fomina M, Liang X (2014) Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol Rev 28:36–55. https://doi.org/10.1016/j.fbr.2014.05.001
Gniadek A, Krzyściak P, Twarużek M, Macura AB (2017) Occurrence of fungi cytotoxicity of the species: Aspergillus ochraceus, Aspergillus niger and Aspergillus flavus isolated from air of hospital wards. Int J Occup Med Environ Health 30(2):231–239. https://doi.org/10.13075/ijomeh.1896.00841
Goldberg IR, Tokem JS, Pines O (2006) Review. Organic acids: old metabolites, new themes. J Chem Technol Biotechnol 81:1601–1611. https://doi.org/10.1002/jctb.1590
Ilondu EM, Nweke OC (2016) Studies on the mycoflora of the outdoor air environemnt of Delta State Unibersity Site III, Abraka, Nigeria. J Chem Biochem 4(1):47–61. https://doi.org/10.15640/jcb.v4n1a4
Karaffa L, Kubicek CP (2003) Aspergillus niger citric acid accumulation: do we understand this well working black box? Appl Microbiol Biotechnol 61:89–196. https://doi.org/10.1007/s00253-002-1201-7
Kishore G, Sugumaran M, Vaidyanathan CS (1976) Metabolism of DL-(+/-)-phenylalanine by Aspergillus niger. J Bacteriol 128(1):182–191
Krebs HA (1970) Rate control of the tricarboxylic acid cycle. Adv Enzym Regul 8:335–353. https://doi.org/10.1016/0065-2571(70)90028-2
Kristiansen B, Sinclair CG (1978) Production of citric acid in batch culture. Biotechnol Bioeng 20:1711–1722. https://doi.org/10.1002/bit.260201103
Kubicek CP (1987) The role of the citric acid cycle in fungal organic acid fermentations. Biochem Soc Symp 54:113–126
Kubicek CP, Zehentgruber O, Röhr M (1979) An indirect method for studying the fine control of citric acid formation by Aspergillus niger. Biotechnol Lett 1:47–52. https://doi.org/10.1007/BF01395790
Kubicek CP, Röhr M, Rehm HJ (1985) Citric acid fermentation. Critical Rev Biotechnol 3:331–373
Kubicek CP, Schreferl-Kunar G, Wöhrer W, Röhr M (1988) Evidence for a cytoplasmic pathway of oxalate biosynthesis in Aspergillus niger. Appl Environ Microbiol 54:633
Kubicek CP, Witteveen CFB, Visser J (1994) Regulation of organic acid production by Aspergilli. In: Powell KA, Renwick A, Peberdy JF (eds) The genus Aspergillus: From taxonomy and genetics to industrial application. Springer US, Boston, pp 135–145
Kuivanen J, Richard P (2017) NADPH-dependent 5-keto-D-gluconate reductase is a part of the fungal pathway for D-glucuronate catabolism. FEBS Lett 592(1):71–77. https://doi.org/10.1002/1873-3468.12946
Kuivanen J, Sugai-Guérios MH, Arvas M, Richard P (2016) A novel pathway for fungal D-glucuronate catabolism contains an L-idonate forming 2-keto-L-gulonate reductase. Sci Rep 6:26329. https://doi.org/10.1038/srep26329
Kuorelahti S, Kalkkinen N, Penttilä M, Londesborough J, Richard P (2005) Identification in the mold Hypocrea jecorina of the first fungal D-galacturonic acid reductase. Biochemistry 44(33):11234–11240
Lee MY, Park HM, Son GH, Lee ChH (2013) Liquid chromatography-mass spectrometry-based chemotaxonomic classification of Aspergillus spp. and evaluation of the biological activity of its unique metabolite, neosartorin. J Microbiol Biotechnol 23(7):932–941. https://doi.org/10.4014/jmb.1212.12068
Li A, van Luijk N, ter Beek M, Caspers M, Punt P, van der Werf M (2011) A clone-based transcriptomics approach for the identification of genes relevant for itaconic acid production in Aspergillus. Fungal Genet Biol 48:602–611. https://doi.org/10.1016/j.fgb.2011.01.013
Li Z, Bai T, Dai L, Wang F, Tao J, Meng S, Hu X, Wang S, Hu S (2016) A study of organic acid production in contrasts between two phosphate solubilization fungi: Penicillium oxalicum and Aspergillus niger. Sci Rep 6:25303/. https://doi.org/10.1038/srep25313
Liaud N, Giniés Ch, Navarro D, Fabre N, Crapant S, Herpoël-Gimbert A, Raouche S, Sigoillot JC (2014) Exploring fungal biodiversity. Organic acids production by 66 strains of filamentous fungi. Fungal Biol Biotech 1:1. http://www.fungalbiolbiotech.com/content/1/1/1
Lockwood LB (1975) Organic acid production in the filamentous fungi. In: Smith HE, Berry DE (eds) Industrial Mycology. Edward Arnold (Pub.) Ltd, London
Matthews S, Halimi M (2015) Gluconic acid production by bacteria to liberate phosphorus from insoluble phosphate complexes. J Trop Agric Fd Sc 43(1):41–53 ESSN: 2289–9650
Mischak H, Kubicek CP, Röhr M (1985) Formation and location of glucose oxidase in citric acid producing mycelia of Aspergillus niger. Appl Microbiol Biotechnol 21:27–31. https://doi.org/10.1007/BF00252357
Mohammadian E, Ahar AB, Arzanlou M, Oustan S, Khazaei SH (2017) Tolerance to heavy metals in filamentous fungi isolated from contaminated mining soils in the Zanjan Province Iran. Chemosphere 185:290–296. https://doi.org/10.1016/j.chemosphere.2017.07.022
Mohanty S, Ghosh S, Nayak S, Das AP (2017) Bioleaching of manganese by Aspergillus sp. Isolated from mining deposits. Chemosphere 172:302–309. https://doi.org/10.1016/j.chemosphere.2016.12.136
Odoni DI, van Gaal MP, Schonewille T, Tamayo-Ramos JA, Martins dos Santos VAP, Suarez-Diesz M, Schaap P (2017) Aspergillus niger secretes citrate to increase iron bioavailability. Front Microbiol 8:1424. https://doi.org/10.3389/fmicb.2017.01424
Pangallo D, Kraková L, Chovanová K, Šimonovičová A, De Leo F, Urzì C (2012) Analysis and comparison of the microflora isolated from fresco surface and from surrounding air environment through molecular and biodegradative assays. World J Microbiol Biotechnol 28(5):2015–2027. https://doi.org/10.1007/s11274-012-1004-7
Papagianni M (2007) Advances in citric acid fermentation by Aspergillus niger: Biochemical aspects, membrane transport and modeling. Biotechnol Adv 25:244–263. https://doi.org/10.1016/jbiotechadv.2007.01.002
Qayyum S, Khan I, Maqbool F, Zhao Y, Gu Q, Peng Ch (2016) Isolation and characterization of heavy metal resistant fungal isolates from industrial soil in China. Pak J Zool 48(5):1241–1247.
Ramachandran S, Fontanille P, Pandey A, Larroche Ch (2006) Gluconic acid: A review. Food Technol Biotechnol 44(2):185–195 (ISSN 1330–9862)
Remenarova M, Takacova A, Šimonovičová A, Danč L, Nosalj S (2020) Reduction of nickel content from the model solution by consortium of fungal pellets and green algae. IOP Conf Series: Earth Environ Sci 444:012047. https://doi.org/10.1088/1755-1315/444/1/012047
Ren WX, Li PJ, Geng Y, Li XJ (2009) Biological leaching of heavy metals from a contaminated soil by Aspergillus niger. J Hazard Mater 167:164–169. https://doi.org/10.1016/j.jhazmat.2008.12.104
Rodrigues AG (2016) Secondary metabolism and antimicrobial metabolites of Aspergillus. In: Gupta VK (ed) New and future developments in microbial biotechnology and bioengineering. Aspergillus system properties and applications. Elsevier BV, Amsterdam, pp 81–93. ISBN: 978-0-444-63505-1
Ruijter GJG, van de Vondervoort PJI, Visser J (1999) Oxalic acid production by Aspergillus niger: an oxalate-non-producing mutant produces citric acid at pH 5 and in the presence of manganese. Microbiol 145:2569–2576. https://doi.org/10.1099/00221287-145-9-2569
Schrickx JM, Raedts MJH, Stouthamer AH, Vanverseveld HW (1995) Organic acid production by Aspergillus niger in recycling culture analyzed by capillary electrophoresis. Anal Biochem 231:175–181. https://doi.org/10.1006/abio.1995.1518
Shivakumar CK, Thippeswamy B, Krishnappa M (2014) Optimization of heavy metals bioaccumulation in Aspergillus niger and Aspergillus flavus. Int J Environ Biol 4(2):188–195. http://urpjournals.com/tocjnls/13_14v4i2_15.pdf
Show PL, Oladele KO, Siew QY, Aziz Zakry FA, Lan JCW, Ling TC (2015) Overview of citric acid production from Aspergillus niger. Front Life Sci 8:271–283. https://doi.org/10.1080/21553769.2015.1033653
Šimonovičová A, Hlinková E, Chovanová K, Pangallo D (2013) Influence of the environment on the morphological and biochemical characteristics of different Aspergillus niger wild type strains. Indian J Microbiol 53(2):187–193. https://doi.org/10.1007/s12088-012-0317-4
Šimonovičová A, Peťková K, Jurkovič Ľ, Ferianc P, Vojtková H, Remenár M, Kraková L, Pangallo D, Hiller E, Čerňanský S (2016) Autochthonous microbiota in arsenic-bearing Technosols from Zemianske Kostoľany (Slovakia) and its potential for bioleaching and biovolatilization of arsenic. Water Air Soil Pollut 227(9):336. https://doi.org/10.1007/s11270-016-3038-1
Šimonovičová A, Ferianc P, Vojtková H, Pangallo D, Hanajík P, Kraková L, Feketeová Z, Čerňanský S, Okenicová L, Žemberyová M, Bujdoš M, Pauditšová E (2017a) Alkaline Technososls contaminated by former mining activity and its culturable autochthonous microbiota. Chemosphere 171:89–96. https://doi.org/10.1016/j.chemosphere.2016.11.131
Šimonovičová A, Nosalj S, Takáčová A, Mackuľak T, Jesenák K, Čerňanský S (2017b) Responses of Aspergillus niger to selected environmental factors. Nova Biotechnol Chim 16(2):92–98. https://doi.org/10.1515/nbec-2017-0013
Šimonovičová A, Kraková L, Pauditšová E, Pangallo D (2019) Occurrence and diversity of cultivable autochthonous microscopic fungi in substrates of old environmental loads from mining activities in Slovakia. Ecotoxicol Environ Saf 172:194–202. https://doi.org/10.1016/j.ecoenv.2019-01.064
Singh M, Srivastava PK, Verma PC, Kharwar RN, Singh N, Tripathi RD (2015) Soil fungi for mycoremediation of arsenic pollution in agriculture soils. J Appl Microbiol 119:1278–1290. https://doi.org/10.1111/jam.12948
Upton DJ, McQeen-Mason SJ, Wood AJ (2017) An accurate description of Aspergillus niger organic acid batch fermentation through dynamic metabolic modelling. Biotechnol Biofuels 10:258. https://doi.org/10.1186/s13068-017-0950-6
Urík M, Bujdoš M, Milová-Žiaková B, Mikušová P, Slovák M, Matúš P (2015) Aluminium leaching from red mud by filamentous fungi. J Inorg Biochem 152:154–159. https://doi.org/10.1016/j.jinorgbio.2015.08.022
Urík M, Polák F, Bujdoš M, Pifková I, Kořenková L, Littera P, Matúš P (2017) Aluminium leaching by heterotrophic microorganism Aspergillus niger: An acidic leaching? Arab J Sci Eng. https://doi.org/10.1007/s13369-017-2784-8
Walaszczyk E, Podgórski W, Janczar-Smuga M, Dymarsla E (2018) Effect of medium pH on chemical selectivity of oxalic acid biosynthesis by Aspergillus niger W78C in submerged cultures with sucrose as a carbon source. Chem Pap 72:1089–1093. https://doi.org/10.1007/s11696-017-0354-x
Witteveen CFB, Veenhuis M, Visser J (1992) Localization of glucose oxidase and catalase activities in Aspergillus niger. Appl Environ Microbiol 58:1190–1194. PMID: 16348689
Wolschek MF, Kubicek CP (1999) Biochemistry of citric acid accumulation by Aspergillus niger. In: Kristiansen B, Mattey M, Linden J (eds) Citric acid biotechnology. Taylor and Francis, London, pp 11–33
Yang L, Lübeck M, Lübeck PS (2017) Aspergillus as a versatile cell factory for organic acid production. Fungal Biol Rev 31:33–49. https://doi.org/10.1016/j.fbr.2016.11.001
Zakes BL (1969) The metabolism of D-Glucaric Acid by Aspergillus niger. Master’s Theses. Loyola University Chicago. https://ecommons.luc.edu/luc_theses/2351
Zeng XZ, Wei S, Sun L, Jacques DA, Tang J, Lian M, Ji Z, Wang J, Zhu J, Xu Z (2015) Bioleaching of heavy metals from contaminated sediments by the Aspergillus niger strain SY1. J Soil Sediment 15:1029–1038. https://doi.org/10.1007/s11368-015-1076-8
Acknowledgements
The work was supported by Slovak National Grant Agency VEGA 1/0424/18, VEGA 2/0142/19, and the Operational Programme Research and Development through the project: Centre of Excellence for Integrated Research of the Earth’s Geosphere (ITMS: 26220120064).
This work was supported by the Project for Specific University Research (SGS) No. SP2020/3 from the Faculty of Mining and Geology of VŠB – Technical University of Ostrava & Ministry of Education, Youth and Sports of the Czech Republic.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Šimonovičová, A., Kupka, D., Nosalj, S. et al. Differences in metabolites production using the Biolog FF Microplate™ system with an emphasis on some organic acids of Aspergillus niger wild type strains. Biologia 75, 1537–1546 (2020). https://doi.org/10.2478/s11756-020-00521-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-020-00521-y