Initial pH determines the morphological characteristics and secondary metabolite production in Aspergillus terreus and Streptomyces rimosus cocultures.


Journal

Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427

Informations de publication

Date de publication:
01 Nov 2024
Historique:
received: 23 07 2024
accepted: 26 10 2024
revised: 10 10 2024
medline: 1 11 2024
pubmed: 1 11 2024
entrez: 1 11 2024
Statut: epublish

Résumé

The influence of the initial pH on the morphology and secondary metabolite production in cocultures and axenic cultures of Aspergillus terreus and Streptomyces rimosus was investigated. The detected secondary metabolites (6 of bacterial and 4 of fungal origin) were not found in the cultures initiated at pH values less than or equal to 4.0. The highest mean levels of oxytetracycline were recorded in S. rimosus axenic culture at pH 5.0. Initiating the axenic culture at pH 5.9 led to visibly lower product levels, yet the presence of A. terreus reduced the negative effect of non-optimal pH and led to higher oxytetracycline titer than in the corresponding S. rimosus axenic culture. The cocultivation initiated at pH 5.0 or 5.9 triggered the formation of oxidized rimocidin. The products of A. terreus were absent in the cocultures. At pH 4.0, the striking morphological differences between the coculture and the axenic cultures were recorded.

Identifiants

pubmed: 39485516
doi: 10.1007/s00203-024-04186-y
pii: 10.1007/s00203-024-04186-y
doi:

Substances chimiques

Culture Media 0
Oxytetracycline X20I9EN955

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

452

Subventions

Organisme : Narodowe Centrum Nauki
ID : 2017/27/B/NZ9/00534
Organisme : Narodowe Centrum Nauki
ID : 2017/27/B/NZ9/00534

Informations de copyright

© 2024. The Author(s).

Références

Amr K, Ibrahim N, Elissawy AM, Singab ANB (2023) Unearthing the fungal endophyte Aspergillus terreus for chemodiversity and medicinal prospects: a comprehensive review. Fungal Biol Biotechnol 10:6
doi: 10.1186/s40694-023-00153-2 pubmed: 36966331 pmcid: 10040139
Arora D, Gupta P, Jaglan S et al (2020) Expanding the chemical diversity through microorganisms co-culture: current status and outlook. Biotechnol Adv 40:107521
doi: 10.1016/j.biotechadv.2020.107521 pubmed: 31953204
Baral B, Akhgari A, Metsä-Ketelä M (2018) Activation of microbial secondary metabolic pathways: avenues and challenges. Synth Syst Biotechnol 3:163–178
doi: 10.1016/j.synbio.2018.09.001 pubmed: 30345402 pmcid: 6190515
Bertrand S, Bohni N, Schnee S et al (2014) Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv 32:1180–1204
doi: 10.1016/j.biotechadv.2014.03.001 pubmed: 24651031
Bizukojć M, Ledakowicz S (2010) The morphological and physiological evolution of Aspergillus terreus mycelium in the submerged culture and its relation to the formation of secondary metabolites. World J Microbiol Biotechnol 26:41–54
doi: 10.1007/s11274-009-0140-1
Bizukojć M, Pawlak M, Boruta T, Gonciarz J (2012) Effect of pH on biosynthesis of lovastatin and other secondary metabolites by Aspergillus terreus ATCC 20542. J Biotechnol 162:253–261
doi: 10.1016/j.jbiotec.2012.09.007 pubmed: 22995742
Boruta T, Bizukojć M (2016) Induction of secondary metabolism of Aspergillus terreus ATCC 20542 in the batch bioreactor cultures. Appl Microbiol Biotechnol 100:3009–3022
doi: 10.1007/s00253-015-7157-1 pubmed: 26603760
Boruta T, Ścigaczewska A, Bizukojć M (2021) Microbial wars in a stirred tank bioreactor: Investigating the co-cultures of Streptomyces rimosus and Aspergillus terreus, filamentous microorganisms equipped with a rich arsenal of secondary metabolites. Front Bioeng Biotechnol 9:713639
doi: 10.3389/fbioe.2021.713639 pubmed: 34660550 pmcid: 8511322
Boruta T, Englart G, Foryś M, Pawlikowska W (2024) The repertoire and levels of secondary metabolites in microbial cocultures depend on the inoculation ratio: a case study involving Aspergillus terreus and Streptomyces rimosus. Biotechnol Lett 46:601–614
doi: 10.1007/s10529-024-03500-4 pubmed: 38844646 pmcid: 11217084
Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32
doi: 10.1038/nrmicro2916 pubmed: 23178386
Carlsen M, Spohr AB, Nielsen J, Villadsen J (1996) Morphology and physiology of an α-amylase producing strain of Aspergillus oryzae during batch cultivations. Biotechnol Bioeng 49:266–276
doi: 10.1002/(SICI)1097-0290(19960205)49:3<266::AID-BIT4>3.0.CO;2-I pubmed: 18623577
Diender M, Parera Olm I, Sousa DZ (2021) Synthetic co-cultures: novel avenues for bio-based processes. Curr Opin Biotechnol 67:72–79
doi: 10.1016/j.copbio.2021.01.006 pubmed: 33517194
Fleming A (1929) On the antibacterial action of cultures of a Penicillium, with special reference to their use in the isolation of B. influenzae. Br J Exp Pathol 10:226–236
pmcid: 2048009
Goers L, Freemont P, Polizzi KM (2014) Co-culture systems and technologies: taking synthetic biology to the next level. J R Soc Interface 11:20140065
doi: 10.1098/rsif.2014.0065 pubmed: 24829281 pmcid: 4032528
Grimm LH, Kelly S, Völkerding II et al (2005) Influence of mechanical stress and surface interaction on the aggregation of Aspergillus niger conidia. Biotechnol Bioeng 92:879–888
doi: 10.1002/bit.20666 pubmed: 16255057
Guo CJ, Wang CCC (2014) Recent advances in genome mining of secondary metabolites in Aspergillus terreus. Front Microbiol 5:124539
doi: 10.3389/fmicb.2014.00717
Kapoore RV, Padmaperuma G, Maneein S, Vaidyanathan S (2022) Co-culturing microbial consortia: approaches for applications in biomanufacturing and bioprocessing. Crit Rev Biotechnol 42:46–72
doi: 10.1080/07388551.2021.1921691 pubmed: 33980092
Keller NP (2019) Fungal secondary metabolism: regulation, function and drug discovery. Nat Rev Microbiol 17:167–180
doi: 10.1038/s41579-018-0121-1 pubmed: 30531948 pmcid: 6381595
Metz B, Kossen NWF (1977) The growth of molds in the form of pellets–a literature review. Biotechnol Bioeng 19:781–799
doi: 10.1002/bit.260190602
Meyer V, Cairns T, Barthel L et al (2021) Understanding and controlling filamentous growth of fungal cell factories: novel tools and opportunities for targeted morphology engineering. Fungal Biol Biotechnol 8:8
doi: 10.1186/s40694-021-00115-6 pubmed: 34425914 pmcid: 8383395
Nai C, Meyer V (2018) From axenic to mixed cultures: Technological advances accelerating a paradigm shift in Microbiology. Trends Microbiol 26:538–554
doi: 10.1016/j.tim.2017.11.004 pubmed: 29191399
Nielsen JC, Nielsen J (2017) Development of fungal cell factories for the production of secondary metabolites: linking genomics and metabolism. Synth Syst Biotechnol 2:5–12
doi: 10.1016/j.synbio.2017.02.002 pubmed: 29062956 pmcid: 5625732
Nyman J, Lacintra MG, Westman JO et al (2013) Pellet formation of zygomycetes and immobilization of yeast. N Biotechnol 30:516–522
doi: 10.1016/j.nbt.2013.05.007 pubmed: 23711366
Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259
doi: 10.1016/j.biotechadv.2003.09.005 pubmed: 14665401
Pšeničnik A, Slemc L, Avbelj M et al (2024) Oxytetracycline hyper-production through targeted genome reduction of Streptomyces rimosus. mSystems 16:e0025024
doi: 10.1128/msystems.00250-24
Ramírez-Rendon D, Passari AK, Ruiz-Villafán B et al (2022) Impact of novel microbial secondary metabolites on the pharma industry. Appl Microbiol Biotechnol 106:1855–1878
doi: 10.1007/s00253-022-11821-5 pubmed: 35188588 pmcid: 8860141
Selegato DM, Castro-Gamboa I (2023) Enhancing chemical and biological diversity by co-cultivation. Front Microbiol 14:1117559
doi: 10.3389/fmicb.2023.1117559 pubmed: 36819067 pmcid: 9928954
Van Santen JA, Poynton EF, Iskakova D et al (2022) The Natural products Atlas 2.0: a database of microbially-derived natural products. Nucleic Acids Res 50:D1317–D1323
doi: 10.1093/nar/gkab941 pubmed: 34718710
Vecht-Lifshitz SE, Magdassi S, Braun S (1990) Pellet formation and cellular aggregation in Streptomyces tendae. Biotechnol Bioeng 35:890–896
doi: 10.1002/bit.260350906 pubmed: 18592593
Veiter L, Rajamanickam V, Herwig C (2018) The filamentous fungal pellet—relationship between morphology and productivity. Appl Microbiol Biotechnol 102:2997–3006
doi: 10.1007/s00253-018-8818-7 pubmed: 29473099 pmcid: 5852183
Wargenau A, Fleißner A, Bolten CJ et al (2011) On the origin of the electrostatic surface potential of Aspergillus niger spores in acidic environments. Res Microbiol 162:1011–1017
doi: 10.1016/j.resmic.2011.07.006 pubmed: 21835241
Wargenau A, Kampen I, Kwade A (2013) Linking aggregation of Aspergillus niger spores to surface electrostatics: a theoretical approach. Biointerphases 8:1–12
doi: 10.1186/1559-4106-8-7
Xia C, Zhang J, Zhang W, Hu B (2011) A new cultivation method for microbial oil production: cell pelletization and lipid accumulation by Mucor circinelloides. Biotechnol Biofuels 4:15
doi: 10.1186/1754-6834-4-15 pubmed: 21635739 pmcid: 3127746
Zhou Y, Du J, Tsao GT (2000) Mycelial Pellet formation by Rhizopus oryzae ATCC 20344. Appl Biochem Biotechnol 84 – 86:779 – 89

Auteurs

Tomasz Boruta (T)

Faculty of Process and Environmental Engineering, Department of Bioprocess Engineering, Lodz University of Technology, ul. Wólczańska 213, Łódź, 93-005, Poland. tomasz.boruta@p.lodz.pl.

Martyna Foryś (M)

Faculty of Process and Environmental Engineering, Department of Bioprocess Engineering, Lodz University of Technology, ul. Wólczańska 213, Łódź, 93-005, Poland.

Weronika Pawlikowska (W)

Faculty of Process and Environmental Engineering, Department of Bioprocess Engineering, Lodz University of Technology, ul. Wólczańska 213, Łódź, 93-005, Poland.

Grzegorz Englart (G)

Faculty of Process and Environmental Engineering, Department of Bioprocess Engineering, Lodz University of Technology, ul. Wólczańska 213, Łódź, 93-005, Poland.

Marcin Bizukojć (M)

Faculty of Process and Environmental Engineering, Department of Bioprocess Engineering, Lodz University of Technology, ul. Wólczańska 213, Łódź, 93-005, Poland.

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