The Streptomyces coelicolor Small ORF trpM Stimulates Growth and Morphological Development and Exerts Opposite Effects on Actinorhodin and Calcium-Dependent Antibiotic Production.
Identifieur interne : 000064 ( Main/Exploration ); précédent : 000063; suivant : 000065The Streptomyces coelicolor Small ORF trpM Stimulates Growth and Morphological Development and Exerts Opposite Effects on Actinorhodin and Calcium-Dependent Antibiotic Production.
Auteurs : Alberto Vassallo [Italie] ; Emilia Palazzotto [Danemark] ; Giovanni Renzone [Italie] ; Luigi Botta [Italie] ; Teresa Faddetta [Italie] ; Andrea Scaloni [Italie] ; Anna Maria Puglia [Italie] ; Giuseppe Gallo [Italie]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2020.
Abstract
In actinomycetes, antibiotic production is often associated with a morpho-physiological differentiation program that is regulated by complex molecular and metabolic networks. Many aspects of these regulatory circuits have been already elucidated and many others still deserve further investigations. In this regard, the possible role of many small open reading frames (smORFs) in actinomycete morpho-physiological differentiation is still elusive. In Streptomyces coelicolor, inactivation of the smORF trpM (SCO2038) - whose product modulates L-tryptophan biosynthesis - impairs production of antibiotics and morphological differentiation. Indeed, it was demonstrated that TrpM is able to interact with PepA (SCO2179), a putative cytosol aminopeptidase playing a key role in antibiotic production and sporulation. In this work, a S. coelicolor trpM knock-in (Sco-trpMKI) mutant strain was generated by cloning trpM into overexpressing vector to further investigate the role of trpM in actinomycete growth and morpho-physiological differentiation. Results highlighted that trpM: (i) stimulates growth and actinorhodin (ACT) production; (ii) decreases calcium-dependent antibiotic (CDA) production; (iii) has no effect on undecylprodigiosin production. Metabolic pathways influenced by trpM knock-in were investigated by combining two-difference in gel electrophoresis/nanoliquid chromatography coupled to electrospray linear ion trap tandem mass spectrometry (2D-DIGE/nanoLC-ESI-LIT-MS/MS) and by LC-ESI-MS/MS procedures, respectively. These analyses demonstrated that over-expression of trpM causes an over-representation of factors involved in protein synthesis and nucleotide metabolism as well as a down-representation of proteins involved in central carbon and amino acid metabolism. At the metabolic level, this corresponded to a differential accumulation pattern of different amino acids - including aromatic ones but tryptophan - and central carbon intermediates. PepA was also down-represented in Sco-trpMKI. The latter was produced as recombinant His-tagged protein and was originally proven having the predicted aminopeptidase activity. Altogether, these results highlight the stimulatory effect of trpM in S. coelicolor growth and ACT biosynthesis, which are elicited through the modulation of various metabolic pathways and PepA representation, further confirming the complexity of regulatory networks that control antibiotic production in actinomycetes.
DOI: 10.3389/fmicb.2020.00224
PubMed: 32140146
PubMed Central: PMC7042404
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The <i>Streptomyces coelicolor</i> Small ORF <i>trpM</i> Stimulates Growth and Morphological Development and Exerts Opposite Effects on Actinorhodin and Calcium-Dependent Antibiotic Production.</title><author><name sortKey="Vassallo, Alberto" sort="Vassallo, Alberto" uniqKey="Vassallo A" first="Alberto" last="Vassallo">Alberto Vassallo</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo</wicri:regionArea><wicri:noRegion>Palermo</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Microbial and Molecular Evolution, Department of Biology, University of Florence, Sesto Fiorentino, 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Development and Exerts Opposite Effects on Actinorhodin and Calcium-Dependent Antibiotic Production.</title><author><name sortKey="Vassallo, Alberto" sort="Vassallo, Alberto" uniqKey="Vassallo A" first="Alberto" last="Vassallo">Alberto Vassallo</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo</wicri:regionArea><wicri:noRegion>Palermo</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Microbial and Molecular Evolution, Department of Biology, University of Florence, Sesto Fiorentino, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Laboratory of Microbial and Molecular Evolution, Department of Biology, University of Florence, Sesto Fiorentino</wicri:regionArea><wicri:noRegion>Sesto Fiorentino</wicri:noRegion></affiliation></author><author><name sortKey="Palazzotto, Emilia" sort="Palazzotto, Emilia" uniqKey="Palazzotto E" first="Emilia" last="Palazzotto">Emilia Palazzotto</name><affiliation wicri:level="1"><nlm:affiliation>Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby</wicri:regionArea><wicri:noRegion>Lyngby</wicri:noRegion></affiliation></author><author><name sortKey="Renzone, Giovanni" sort="Renzone, Giovanni" uniqKey="Renzone G" first="Giovanni" last="Renzone">Giovanni Renzone</name><affiliation wicri:level="1"><nlm:affiliation>Proteomic and Mass Spectrometry Laboratory, ISPAAM, National Research Council, Naples, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Proteomic and Mass Spectrometry Laboratory, ISPAAM, National Research Council, Naples</wicri:regionArea><wicri:noRegion>Naples</wicri:noRegion></affiliation></author><author><name sortKey="Botta, Luigi" sort="Botta, Luigi" uniqKey="Botta L" first="Luigi" last="Botta">Luigi Botta</name><affiliation wicri:level="4"><nlm:affiliation>Dipartimento di Ingegneria, Università di Palermo, Palermo, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Ingegneria, Università di Palermo, Palermo</wicri:regionArea><orgName type="university">Université de Palerme</orgName><placeName><settlement type="city">Palerme</settlement><region type="region" nuts="2">Sicile</region></placeName></affiliation></author><author><name sortKey="Faddetta, Teresa" sort="Faddetta, Teresa" uniqKey="Faddetta T" first="Teresa" last="Faddetta">Teresa Faddetta</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo</wicri:regionArea><wicri:noRegion>Palermo</wicri:noRegion></affiliation></author><author><name sortKey="Scaloni, Andrea" sort="Scaloni, Andrea" uniqKey="Scaloni A" first="Andrea" last="Scaloni">Andrea Scaloni</name><affiliation wicri:level="1"><nlm:affiliation>Proteomic and Mass Spectrometry Laboratory, ISPAAM, National Research Council, Naples, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Proteomic and Mass Spectrometry Laboratory, ISPAAM, National Research Council, Naples</wicri:regionArea><wicri:noRegion>Naples</wicri:noRegion></affiliation></author><author><name sortKey="Puglia, Anna Maria" sort="Puglia, Anna Maria" uniqKey="Puglia A" first="Anna Maria" last="Puglia">Anna Maria Puglia</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo</wicri:regionArea><wicri:noRegion>Palermo</wicri:noRegion></affiliation></author><author><name sortKey="Gallo, Giuseppe" sort="Gallo, Giuseppe" uniqKey="Gallo G" first="Giuseppe" last="Gallo">Giuseppe Gallo</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo</wicri:regionArea><wicri:noRegion>Palermo</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">In actinomycetes, antibiotic production is often associated with a morpho-physiological differentiation program that is regulated by complex molecular and metabolic networks. Many aspects of these regulatory circuits have been already elucidated and many others still deserve further investigations. In this regard, the possible role of many small open reading frames (smORFs) in actinomycete morpho-physiological differentiation is still elusive. In <i>Streptomyces coelicolor</i>, inactivation of the smORF <i>trpM</i> (SCO2038) - whose product modulates L-tryptophan biosynthesis - impairs production of antibiotics and morphological differentiation. Indeed, it was demonstrated that TrpM is able to interact with PepA (SCO2179), a putative cytosol aminopeptidase playing a key role in antibiotic production and sporulation. In this work, a <i>S. coelicolor trpM</i> knock-in (Sco-<i>trpM</i>KI) mutant strain was generated by cloning <i>trpM</i> into overexpressing vector to further investigate the role of <i>trpM</i> in actinomycete growth and morpho-physiological differentiation. Results highlighted that <i>trpM</i>: (i) stimulates growth and actinorhodin (ACT) production; (ii) decreases calcium-dependent antibiotic (CDA) production; (iii) has no effect on undecylprodigiosin production. Metabolic pathways influenced by <i>trpM</i> knock-in were investigated by combining two-difference in gel electrophoresis/nanoliquid chromatography coupled to electrospray linear ion trap tandem mass spectrometry (2D-DIGE/nanoLC-ESI-LIT-MS/MS) and by LC-ESI-MS/MS procedures, respectively. These analyses demonstrated that over-expression of <i>trpM</i> causes an over-representation of factors involved in protein synthesis and nucleotide metabolism as well as a down-representation of proteins involved in central carbon and amino acid metabolism. At the metabolic level, this corresponded to a differential accumulation pattern of different amino acids - including aromatic ones but tryptophan - and central carbon intermediates. PepA was also down-represented in Sco-<i>trpM</i>KI. The latter was produced as recombinant His-tagged protein and was originally proven having the predicted aminopeptidase activity. Altogether, these results highlight the stimulatory effect of <i>trpM</i> in <i>S. coelicolor</i> growth and ACT biosynthesis, which are elicited through the modulation of various metabolic pathways and PepA representation, further confirming the complexity of regulatory networks that control antibiotic production in actinomycetes.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32140146</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>The <i>Streptomyces coelicolor</i> Small ORF <i>trpM</i> Stimulates Growth and Morphological Development and Exerts Opposite Effects on Actinorhodin and Calcium-Dependent Antibiotic Production.</ArticleTitle><Pagination><MedlinePgn>224</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2020.00224</ELocationID><Abstract><AbstractText>In actinomycetes, antibiotic production is often associated with a morpho-physiological differentiation program that is regulated by complex molecular and metabolic networks. Many aspects of these regulatory circuits have been already elucidated and many others still deserve further investigations. In this regard, the possible role of many small open reading frames (smORFs) in actinomycete morpho-physiological differentiation is still elusive. In <i>Streptomyces coelicolor</i>, inactivation of the smORF <i>trpM</i> (SCO2038) - whose product modulates L-tryptophan biosynthesis - impairs production of antibiotics and morphological differentiation. Indeed, it was demonstrated that TrpM is able to interact with PepA (SCO2179), a putative cytosol aminopeptidase playing a key role in antibiotic production and sporulation. In this work, a <i>S. coelicolor trpM</i> knock-in (Sco-<i>trpM</i>KI) mutant strain was generated by cloning <i>trpM</i> into overexpressing vector to further investigate the role of <i>trpM</i> in actinomycete growth and morpho-physiological differentiation. Results highlighted that <i>trpM</i>: (i) stimulates growth and actinorhodin (ACT) production; (ii) decreases calcium-dependent antibiotic (CDA) production; (iii) has no effect on undecylprodigiosin production. Metabolic pathways influenced by <i>trpM</i> knock-in were investigated by combining two-difference in gel electrophoresis/nanoliquid chromatography coupled to electrospray linear ion trap tandem mass spectrometry (2D-DIGE/nanoLC-ESI-LIT-MS/MS) and by LC-ESI-MS/MS procedures, respectively. These analyses demonstrated that over-expression of <i>trpM</i> causes an over-representation of factors involved in protein synthesis and nucleotide metabolism as well as a down-representation of proteins involved in central carbon and amino acid metabolism. At the metabolic level, this corresponded to a differential accumulation pattern of different amino acids - including aromatic ones but tryptophan - and central carbon intermediates. PepA was also down-represented in Sco-<i>trpM</i>KI. The latter was produced as recombinant His-tagged protein and was originally proven having the predicted aminopeptidase activity. Altogether, these results highlight the stimulatory effect of <i>trpM</i> in <i>S. coelicolor</i> growth and ACT biosynthesis, which are elicited through the modulation of various metabolic pathways and PepA representation, further confirming the complexity of regulatory networks that control antibiotic production in actinomycetes.</AbstractText><CopyrightInformation>Copyright © 2020 Vassallo, Palazzotto, Renzone, Botta, Faddetta, Scaloni, Puglia and Gallo.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Vassallo</LastName><ForeName>Alberto</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratory of Microbial and Molecular Evolution, Department of Biology, University of Florence, Sesto Fiorentino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Palazzotto</LastName><ForeName>Emilia</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Renzone</LastName><ForeName>Giovanni</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Proteomic and Mass Spectrometry Laboratory, ISPAAM, National Research Council, Naples, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Botta</LastName><ForeName>Luigi</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Dipartimento di Ingegneria, Università di Palermo, Palermo, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Faddetta</LastName><ForeName>Teresa</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Scaloni</LastName><ForeName>Andrea</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Proteomic and Mass Spectrometry Laboratory, ISPAAM, National Research Council, Naples, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Puglia</LastName><ForeName>Anna Maria</ForeName><Initials>AM</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gallo</LastName><ForeName>Giuseppe</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>02</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Streptomyces coelicolor</Keyword><Keyword MajorTopicYN="N">actinorhodin production</Keyword><Keyword MajorTopicYN="N">calcium-dependent antibiotic</Keyword><Keyword MajorTopicYN="N">cytosol aminopeptidase</Keyword><Keyword MajorTopicYN="N">primary and secondary metabolism</Keyword><Keyword MajorTopicYN="N">small open reading frame</Keyword><Keyword MajorTopicYN="N">trpM</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>10</Month><Day>16</Day></PubMedPubDate><PubMedPubDate 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T" first="Teresa" last="Faddetta">Teresa Faddetta</name><name sortKey="Gallo, Giuseppe" sort="Gallo, Giuseppe" uniqKey="Gallo G" first="Giuseppe" last="Gallo">Giuseppe Gallo</name><name sortKey="Puglia, Anna Maria" sort="Puglia, Anna Maria" uniqKey="Puglia A" first="Anna Maria" last="Puglia">Anna Maria Puglia</name><name sortKey="Renzone, Giovanni" sort="Renzone, Giovanni" uniqKey="Renzone G" first="Giovanni" last="Renzone">Giovanni Renzone</name><name sortKey="Scaloni, Andrea" sort="Scaloni, Andrea" uniqKey="Scaloni A" first="Andrea" last="Scaloni">Andrea Scaloni</name><name sortKey="Vassallo, Alberto" sort="Vassallo, Alberto" uniqKey="Vassallo A" first="Alberto" last="Vassallo">Alberto Vassallo</name></country><country name="Danemark"><noRegion><name sortKey="Palazzotto, Emilia" sort="Palazzotto, Emilia" uniqKey="Palazzotto E" first="Emilia" last="Palazzotto">Emilia Palazzotto</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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