Expression of bik cluster and production of bikaverin by Fusarium oxysporum f. sp. lycopersici grown using two alternate nitrogen sources
The genus Fusarium can be utilized to produce a great variety of secondary metabolites under specific culture conditions, including pigments of increasing biotechnological interest, such as bikaverin. Such pigments are important due to the biological properties they possess, including antitumor and...
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Published in: | International microbiology Vol. 25; no. 1; pp. 153 - 164 |
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Language: | English |
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Abstract | The genus
Fusarium
can be utilized to produce a great variety of secondary metabolites under specific culture conditions, including pigments of increasing biotechnological interest, such as bikaverin. Such pigments are important due to the biological properties they possess, including antitumor and antibiotic activities, among others. In
Fusarium fujikuroi
,
bik1–bik6
have been identified as the genes that are responsible for the synthesis of bikaverin. Therefore, in this study, we screened for the presence of
bik
genes and examined changes in mRNA levels of the
bik
genes under the influence of NH
4
NO
3
(0.024, 0.048, 0.50, 1.0, and 4.60 g L
−1
) and NH
4
Cl (0.50 and 1.0 g L
−1
) as nitrogen sources for the phytopathogen
Fusarium oxysporum
f. sp
.
lycopersici
. Our results indicated the presence of at least six
bik
(
bik1–bik6
) genes and showed increased mRNA levels for
bik4
,
bik5
, and
bik6
in conditions where NH
4
NO
3
was used at pH 3.0. The characteristic coloration of bikaverin was obtained in 10 out of 16 culture conditions, except when the fungus was grown with higher concentrations of NH
4
NO
3
(1.0 and 4.60 g L
−1
). The pigment was chloroform-extracted from the culture conditions of NH
4
NO
3
(0.024, 0.048, and 0.50 g L
−1
) and NH
4
Cl (0.50 and 1.0 g L
−1
) with 3 and 9 days of incubation. Analysis via visible spectroscopy and matrix-assisted laser desorption ionization-time of flight mass spectrometry were used for the identification of bikaverin. |
---|---|
AbstractList | The genus Fusarium can be utilized to produce a great variety of secondary metabolites under specific culture conditions, including pigments of increasing biotechnological interest, such as bikaverin. Such pigments are important due to the biological properties they possess, including antitumor and antibiotic activities, among others. In Fusarium fujikuroi, bik1-bik6 have been identified as the genes that are responsible for the synthesis of bikaverin. Therefore, in this study, we screened for the presence of bik genes and examined changes in mRNA levels of the bik genes under the influence of NH
NO
(0.024, 0.048, 0.50, 1.0, and 4.60 g L
) and NH
Cl (0.50 and 1.0 g L
) as nitrogen sources for the phytopathogen Fusarium oxysporum f. sp. lycopersici. Our results indicated the presence of at least six bik (bik1-bik6) genes and showed increased mRNA levels for bik4, bik5, and bik6 in conditions where NH
NO
was used at pH 3.0. The characteristic coloration of bikaverin was obtained in 10 out of 16 culture conditions, except when the fungus was grown with higher concentrations of NH
NO
(1.0 and 4.60 g L
). The pigment was chloroform-extracted from the culture conditions of NH
NO
(0.024, 0.048, and 0.50 g L
) and NH
Cl (0.50 and 1.0 g L
) with 3 and 9 days of incubation. Analysis via visible spectroscopy and matrix-assisted laser desorption ionization-time of flight mass spectrometry were used for the identification of bikaverin. The genus Fusarium can be utilized to produce a great variety of secondary metabolites under specific culture conditions, including pigments of increasing biotechnological interest, such as bikaverin. Such pigments are important due to the biological properties they possess, including antitumor and antibiotic activities, among others. In Fusarium fujikuroi , bik1–bik6 have been identified as the genes that are responsible for the synthesis of bikaverin. Therefore, in this study, we screened for the presence of bik genes and examined changes in mRNA levels of the bik genes under the influence of NH 4 NO 3 (0.024, 0.048, 0.50, 1.0, and 4.60 g L −1 ) and NH 4 Cl (0.50 and 1.0 g L −1 ) as nitrogen sources for the phytopathogen Fusarium oxysporum f. sp . lycopersici . Our results indicated the presence of at least six bik ( bik1–bik6 ) genes and showed increased mRNA levels for bik4 , bik5 , and bik6 in conditions where NH 4 NO 3 was used at pH 3.0. The characteristic coloration of bikaverin was obtained in 10 out of 16 culture conditions, except when the fungus was grown with higher concentrations of NH 4 NO 3 (1.0 and 4.60 g L −1 ). The pigment was chloroform-extracted from the culture conditions of NH 4 NO 3 (0.024, 0.048, and 0.50 g L −1 ) and NH 4 Cl (0.50 and 1.0 g L −1 ) with 3 and 9 days of incubation. Analysis via visible spectroscopy and matrix-assisted laser desorption ionization-time of flight mass spectrometry were used for the identification of bikaverin. The genus Fusarium can be utilized to produce a great variety of secondary metabolites under specific culture conditions, including pigments of increasing biotechnological interest, such as bikaverin. Such pigments are important due to the biological properties they possess, including antitumor and antibiotic activities, among others. In Fusarium fujikuroi, bik1–bik6 have been identified as the genes that are responsible for the synthesis of bikaverin. Therefore, in this study, we screened for the presence of bik genes and examined changes in mRNA levels of the bik genes under the influence of NH4NO3 (0.024, 0.048, 0.50, 1.0, and 4.60 g L−1) and NH4Cl (0.50 and 1.0 g L−1) as nitrogen sources for the phytopathogen Fusarium oxysporum f. sp. lycopersici. Our results indicated the presence of at least six bik (bik1–bik6) genes and showed increased mRNA levels for bik4, bik5, and bik6 in conditions where NH4NO3 was used at pH 3.0. The characteristic coloration of bikaverin was obtained in 10 out of 16 culture conditions, except when the fungus was grown with higher concentrations of NH4NO3 (1.0 and 4.60 g L−1). The pigment was chloroform-extracted from the culture conditions of NH4NO3 (0.024, 0.048, and 0.50 g L−1) and NH4Cl (0.50 and 1.0 g L−1) with 3 and 9 days of incubation. Analysis via visible spectroscopy and matrix-assisted laser desorption ionization-time of flight mass spectrometry were used for the identification of bikaverin. |
Author | Rodríguez-Torres, María Fernanda Gutiérrez-Aguilar, Raymundo Meza-Carmen, Víctor Corrales-Escobosa, Alma Rosa Macías-Sánchez, Karla Lizbeth |
Author_xml | – sequence: 1 givenname: María Fernanda surname: Rodríguez-Torres fullname: Rodríguez-Torres, María Fernanda organization: Unidad Profesional Interdisciplinaria de Ingeniería Campus Guanajuato, Instituto Politécnico Nacional – sequence: 2 givenname: Raymundo surname: Gutiérrez-Aguilar fullname: Gutiérrez-Aguilar, Raymundo organization: Unidad Profesional Interdisciplinaria de Ingeniería Campus Guanajuato, Instituto Politécnico Nacional – sequence: 3 givenname: Alma Rosa orcidid: 0000-0002-7581-4813 surname: Corrales-Escobosa fullname: Corrales-Escobosa, Alma Rosa organization: Departamento de Química, División de Ciencias Naturales y Exactas, Universidad de Guanajuato – sequence: 4 givenname: Víctor orcidid: 0000-0003-2838-7211 surname: Meza-Carmen fullname: Meza-Carmen, Víctor organization: Instituto de Investigaciones Químico Biológicas, Universidad Michoacana de San Nicolás de Hidalgo – sequence: 5 givenname: Karla Lizbeth orcidid: 0000-0002-1059-5955 surname: Macías-Sánchez fullname: Macías-Sánchez, Karla Lizbeth email: kmaciass@ipn.mx organization: Unidad Profesional Interdisciplinaria de Ingeniería Campus Guanajuato, Instituto Politécnico Nacional |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34455510$$D View this record in MEDLINE/PubMed |
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Cites_doi | 10.1186/s13568-016-0205-0 10.1128/EC.00076-08 10.1002/chin.197147360 10.1007/BF03192219 10.1002/btpr.2738 10.1016/S0378-1097(97)00298-X 10.1007/s10438-005-0091-8 10.1111/j.1574-6968.1999.tb13530.x 10.1016/0278-6915(92)90038-M 10.1007/BF02880192 10.3389/fmicb.2014.00656 10.1038/s41467-020-19984-3 10.1186/s40694-017-0033-2 10.1111/j.1365-2958.2009.06695.x 10.1002/cbic.201100132 10.1038/srep21367 10.7164/antibiotics.26.778 10.1016/s1087-1845(02)00501-7 10.1128/mmbr.61.1.17-32.1997 10.1093/nar/25.22.4692 10.1007/978-3-319-19456-1_26-1 |
ContentType | Journal Article |
Copyright | The Author(s), under exclusive licence to Springer Nature Switzerland AG 2021 2021. The Author(s), under exclusive licence to Springer Nature Switzerland AG. Copyright Spanish Society for Microbiology Jan 2022 |
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Keywords | Pigments cluster Naftoquinonas Bikaverin Fusarium Bik cluster |
Language | English |
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References | Balan, Fuska, Kuhr, Kuhrová (CR2) 1970; 15 CR4 Medentsev, Arinbasarova, Akimenko (CR14) 2005; 41 Brewer, Arsenault, Wright, Vining (CR3) 1973; 26 Marzluf (CR13) 1997; 61 Norred, Plattner, Vesonder, Bacon, Voss (CR16) 1992; 30 Tudzynski (CR18) 2014; 28 Gmoser, A. Ferreira J, Lennartsson P, Taherzadeh M (CR8) 2017; 4 Scherlach, Sarkar, Schroeckh, Dahse, Roth, Brakhage, Horn, Hertweck (CR17) 2011; 12 García, Di Pietro, Roncero (CR6) 1997; 154 Lebeau, Petit, Clerc, Dufossé, Caro (CR11) 2019; 35 Wiemann, Willmann, Straeten, Kleigrewe, Beyer, Humpf, Tudzynski (CR19) 2009; 72 Nirmaladevi, Venkataramana, Srivastava, Uppalapati, Gupta, Yli-Mattila, Clement Tsui, Srinivas, Niranjana, Chandra (CR15) 2016; 6 Kjaer, Kjaer, Pedersen, Bu´Lock JD, Smith JR (CR9) 1971; 16 Zhao, Zhao, Yao, Iqbal, Hu, Qiao, Li, Skovbjerg, Nielsen, Jielsen, Frandsen, Yuan, Boeke (CR21) 2020; 11 Aljabani, Martínez (CR1) 1997; 25 Giordano, Avalos, Cerdá-Olmedo, Domenech (CR7) 1999; 173 Linnemannstöns, Schulte, del Mar, Proctor, Avalos, Tudzynski (CR12) 2002; 37 Lale, Gadre (CR10) 2016; 6 Chelkowski, Zajkowski, Visconti (CR5) 1992; 8 Wong, Hynes, Davis (CR20) 2008; 7 J Balan (206_CR2) 1970; 15 J Chelkowski (206_CR5) 1992; 8 GJ Lale (206_CR10) 2016; 6 M Zhao (206_CR21) 2020; 11 WP Norred (206_CR16) 1992; 30 K Scherlach (206_CR17) 2011; 12 D Brewer (206_CR3) 1973; 26 J Lebeau (206_CR11) 2019; 35 GA Marzluf (206_CR13) 1997; 61 D Kjaer (206_CR9) 1971; 16 P Linnemannstöns (206_CR12) 2002; 37 KH Wong (206_CR20) 2008; 7 SM Aljabani (206_CR1) 1997; 25 B Tudzynski (206_CR18) 2014; 28 P Wiemann (206_CR19) 2009; 72 F García (206_CR6) 1997; 154 AG Medentsev (206_CR14) 2005; 41 R Gmoser (206_CR8) 2017; 4 206_CR4 D Nirmaladevi (206_CR15) 2016; 6 W Giordano (206_CR7) 1999; 173 |
References_xml | – volume: 6 start-page: 1 year: 2016 end-page: 11 ident: CR10 article-title: Production of bikaverin by a mutant in submerged cultures publication-title: AMB Express doi: 10.1186/s13568-016-0205-0 contributor: fullname: Gadre – volume: 7 start-page: 917 year: 2008 end-page: 925 ident: CR20 article-title: Recent advances in nitrogen regulation: a comparison between and filamentous fungi publication-title: Eukaryot Cell doi: 10.1128/EC.00076-08 contributor: fullname: Davis – volume: 16 start-page: 2792 year: 1971 end-page: 2797 ident: CR9 article-title: Bikaverin and norbikaverin, benzoxanthentrione pigments of publication-title: J Chem Soc doi: 10.1002/chin.197147360 contributor: fullname: Bu´Lock JD, Smith JR – volume: 8 start-page: 73 year: 1992 end-page: 76 ident: CR5 article-title: Bikaverin production of species publication-title: Mycotoxin Res doi: 10.1007/BF03192219 contributor: fullname: Visconti – volume: 35 year: 2019 ident: CR11 article-title: Isolation of two novel purple naphthoquinone pigments concomitant with the bioactive red bikaverin and derivates thereof produced by publication-title: Biotechnol Prog doi: 10.1002/btpr.2738 contributor: fullname: Caro – volume: 154 start-page: 37 year: 1997 end-page: 43 ident: CR6 article-title: Purification and characterization of a novel exopolygalacturonase from Fusarium oxysporum f. sp. lycopersici publication-title: FEMS Microbiol Lett doi: 10.1016/S0378-1097(97)00298-X contributor: fullname: Roncero – volume: 41 start-page: 503 year: 2005 end-page: 507 ident: CR14 article-title: Biosynthesis of naphthoquinone pigments by fungi of the genus publication-title: Appl Biochem Microbiol doi: 10.1007/s10438-005-0091-8 contributor: fullname: Akimenko – ident: CR4 – volume: 173 start-page: 389 year: 1999 end-page: 393 ident: CR7 article-title: Nitrogen availability and production of bikaverin and gibberellins in publication-title: FEMS Microbiol Lett doi: 10.1111/j.1574-6968.1999.tb13530.x contributor: fullname: Domenech – volume: 30 start-page: 233 year: 1992 end-page: 237 ident: CR16 article-title: Effects of selected secondary metabolites of on unscheduled synthesis of DNA by rat primary hepatocytes publication-title: Food Chem Toxicol doi: 10.1016/0278-6915(92)90038-M contributor: fullname: Voss – volume: 15 start-page: 479 year: 1970 end-page: 484 ident: CR2 article-title: Bikaverin, an antibiotic from , effective against publication-title: Folia Microbiol doi: 10.1007/BF02880192 contributor: fullname: Kuhrová – volume: 28 start-page: 656 year: 2014 ident: CR18 article-title: Nitrogen regulation of fungal secondary metabolism in fungi publication-title: Front Microbiol doi: 10.3389/fmicb.2014.00656 contributor: fullname: Tudzynski – volume: 11 start-page: 6197 year: 2020 ident: CR21 article-title: Pathway engineering in yeast fo synthesizing the complex polyketide bikaverin publication-title: Nat Commun doi: 10.1038/s41467-020-19984-3 contributor: fullname: Boeke – volume: 4 start-page: 1 year: 2017 end-page: 25 ident: CR8 article-title: Filamentous ascomycetes fungi as a source of natural pigments publication-title: Fungal Biol Biotechnol doi: 10.1186/s40694-017-0033-2 contributor: fullname: A. Ferreira J, Lennartsson P, Taherzadeh M – volume: 72 start-page: 931 year: 2009 end-page: 946 ident: CR19 article-title: Biosynthesis of the red pigment bikaverin in : genes, their function and regulation publication-title: Mol Microbiol doi: 10.1111/j.1365-2958.2009.06695.x contributor: fullname: Tudzynski – volume: 12 start-page: 1836 year: 2011 end-page: 1839 ident: CR17 article-title: Two induced fungal polyketide pathways converge into antiproliferative spiroanthrones publication-title: ChemBioChem doi: 10.1002/cbic.201100132 contributor: fullname: Hertweck – volume: 6 start-page: 21367 year: 2016 ident: CR15 article-title: Molecular phylogeny, pathogenicity and toxigenicity of f . sp . publication-title: Sci Rep doi: 10.1038/srep21367 contributor: fullname: Chandra – volume: 26 start-page: 778 year: 1973 end-page: 781 ident: CR3 article-title: Production of bikaverin by and its identity with lycopersin publication-title: J Antibiot doi: 10.7164/antibiotics.26.778 contributor: fullname: Vining – volume: 37 start-page: 134 year: 2002 end-page: 148 ident: CR12 article-title: The polyketide synthase gene pks4 from encodes a key enzyme in the biosynthesis of the red pigment bikaverin publication-title: Fungal Genet Biol doi: 10.1016/s1087-1845(02)00501-7 contributor: fullname: Tudzynski – volume: 61 start-page: 17 year: 1997 end-page: 32 ident: CR13 article-title: Genetic regulation of nitrogen metabolism in the fungi publication-title: Microbiol Mol Biol Rev doi: 10.1128/mmbr.61.1.17-32.1997 contributor: fullname: Marzluf – volume: 25 start-page: 4692 year: 1997 end-page: 4693 ident: CR1 article-title: Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques publication-title: Nucl Acid Res doi: 10.1093/nar/25.22.4692 contributor: fullname: Martínez – volume: 6 start-page: 1 year: 2016 ident: 206_CR10 publication-title: AMB Express doi: 10.1186/s13568-016-0205-0 contributor: fullname: GJ Lale – volume: 28 start-page: 656 year: 2014 ident: 206_CR18 publication-title: Front Microbiol doi: 10.3389/fmicb.2014.00656 contributor: fullname: B Tudzynski – volume: 8 start-page: 73 year: 1992 ident: 206_CR5 publication-title: Mycotoxin Res doi: 10.1007/BF03192219 contributor: fullname: J Chelkowski – volume: 12 start-page: 1836 year: 2011 ident: 206_CR17 publication-title: ChemBioChem doi: 10.1002/cbic.201100132 contributor: fullname: K Scherlach – volume: 173 start-page: 389 year: 1999 ident: 206_CR7 publication-title: FEMS Microbiol Lett doi: 10.1111/j.1574-6968.1999.tb13530.x contributor: fullname: W Giordano – volume: 35 year: 2019 ident: 206_CR11 publication-title: Biotechnol Prog doi: 10.1002/btpr.2738 contributor: fullname: J Lebeau – volume: 25 start-page: 4692 year: 1997 ident: 206_CR1 publication-title: Nucl Acid Res doi: 10.1093/nar/25.22.4692 contributor: fullname: SM Aljabani – volume: 7 start-page: 917 year: 2008 ident: 206_CR20 publication-title: Eukaryot Cell doi: 10.1128/EC.00076-08 contributor: fullname: KH Wong – volume: 11 start-page: 6197 year: 2020 ident: 206_CR21 publication-title: Nat Commun doi: 10.1038/s41467-020-19984-3 contributor: fullname: M Zhao – volume: 72 start-page: 931 year: 2009 ident: 206_CR19 publication-title: Mol Microbiol doi: 10.1111/j.1365-2958.2009.06695.x contributor: fullname: P Wiemann – volume: 4 start-page: 1 year: 2017 ident: 206_CR8 publication-title: Fungal Biol Biotechnol doi: 10.1186/s40694-017-0033-2 contributor: fullname: R Gmoser – ident: 206_CR4 doi: 10.1007/978-3-319-19456-1_26-1 – volume: 16 start-page: 2792 year: 1971 ident: 206_CR9 publication-title: J Chem Soc doi: 10.1002/chin.197147360 contributor: fullname: D Kjaer – volume: 26 start-page: 778 year: 1973 ident: 206_CR3 publication-title: J Antibiot doi: 10.7164/antibiotics.26.778 contributor: fullname: D Brewer – volume: 61 start-page: 17 year: 1997 ident: 206_CR13 publication-title: Microbiol Mol Biol Rev doi: 10.1128/mmbr.61.1.17-32.1997 contributor: fullname: GA Marzluf – volume: 6 start-page: 21367 year: 2016 ident: 206_CR15 publication-title: Sci Rep doi: 10.1038/srep21367 contributor: fullname: D Nirmaladevi – volume: 154 start-page: 37 year: 1997 ident: 206_CR6 publication-title: FEMS Microbiol Lett doi: 10.1016/S0378-1097(97)00298-X contributor: fullname: F García – volume: 41 start-page: 503 year: 2005 ident: 206_CR14 publication-title: Appl Biochem Microbiol doi: 10.1007/s10438-005-0091-8 contributor: fullname: AG Medentsev – volume: 15 start-page: 479 year: 1970 ident: 206_CR2 publication-title: Folia Microbiol doi: 10.1007/BF02880192 contributor: fullname: J Balan – volume: 37 start-page: 134 year: 2002 ident: 206_CR12 publication-title: Fungal Genet Biol doi: 10.1016/s1087-1845(02)00501-7 contributor: fullname: P Linnemannstöns – volume: 30 start-page: 233 year: 1992 ident: 206_CR16 publication-title: Food Chem Toxicol doi: 10.1016/0278-6915(92)90038-M contributor: fullname: WP Norred |
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Snippet | The genus
Fusarium
can be utilized to produce a great variety of secondary metabolites under specific culture conditions, including pigments of increasing... The genus Fusarium can be utilized to produce a great variety of secondary metabolites under specific culture conditions, including pigments of increasing... |
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SubjectTerms | Ammonium chloride Ammonium nitrate Antibiotics Anticancer properties Applied Microbiology Biological properties Biomedical and Life Sciences Chloroform Coloration Eukaryotic Microbiology Fusarium - genetics Fusarium fujikuroi Fusarium oxysporum Genes Ionization Ions Life Sciences Mass spectrometry Mass spectroscopy Medical Microbiology Metabolites Microbial Ecology Microbiology mRNA Nitrogen Nitrogen sources Original Article Pigments Secondary metabolites Xanthones |
Title | Expression of bik cluster and production of bikaverin by Fusarium oxysporum f. sp. lycopersici grown using two alternate nitrogen sources |
URI | https://link.springer.com/article/10.1007/s10123-021-00206-9 https://www.ncbi.nlm.nih.gov/pubmed/34455510 https://www.proquest.com/docview/2622302204 https://search.proquest.com/docview/2566253818 |
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