Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and Exceptions

Streptomycetes are well known antibiotic producers and are among the rare prokaryotes able to store carbon as lipids. Previous comparative studies of the weak antibiotic producer <i>Streptomyces lividans</i> with its <i>ppk</i> mutant and with <i>Streptomyces coelicolor...

Full description

Bibliographic Details
Main Authors: Michelle David, Clara Lejeune, Sonia Abreu, Annabelle Thibessard, Pierre Leblond, Pierre Chaminade, Marie-Joelle Virolle
Format: Article
Language:English
Published: MDPI AG 2020-05-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/9/6/280
_version_ 1797567056666689536
author Michelle David
Clara Lejeune
Sonia Abreu
Annabelle Thibessard
Pierre Leblond
Pierre Chaminade
Marie-Joelle Virolle
author_facet Michelle David
Clara Lejeune
Sonia Abreu
Annabelle Thibessard
Pierre Leblond
Pierre Chaminade
Marie-Joelle Virolle
author_sort Michelle David
collection DOAJ
description Streptomycetes are well known antibiotic producers and are among the rare prokaryotes able to store carbon as lipids. Previous comparative studies of the weak antibiotic producer <i>Streptomyces lividans</i> with its <i>ppk</i> mutant and with <i>Streptomyces coelicolor</i>, which both produce antibiotics, suggested the existence of a negative correlation between total lipid content and the ability to produce antibiotics. To determine whether such a negative correlation can be generalized to other <i>Streptomyces</i> species, fifty-four strains were picked randomly and grown on modified R2YE medium, limited in phosphate, with glucose or glycerol as the main carbon source. The total lipid content and antibiotic activity against <i>Micrococcus luteus</i> were assessed for each strain. This study revealed that the ability to accumulate lipids was not evenly distributed among strains and that glycerol was more lipogenic than glucose and had a negative impact on antibiotic biosynthesis. Furthermore, a statistically significant negative Pearson correlation between lipid content and antibiotic activity could be established for most strains, but a few strains escape this general law. These exceptions are likely due to limits and biases linked to the type of test used to determine antibiotic activity, which relies exclusively on <i>Micrococcus luteus</i> sensitivity. They are characterized either by high lipid content and high antibiotic activity or by low lipid content and undetectable antibiotic activity against <i>Micrococcus luteus</i>. Lastly, the comparative genomic analysis of two strains with contrasting lipid content, and both named <i>Streptomyces antibioticus</i> (DSM 41,481 and DSM 40,868, which we found to be phylogenetically related to <i>Streptomyces lavenduligriseus</i>)<i>,</i> indicated that some genetic differences in various pathways related to the generation/consumption of acetylCoA could be responsible for such a difference.
first_indexed 2024-03-10T19:36:13Z
format Article
id doaj.art-fcefc982a1cf4f9196c52d2f72687535
institution Directory Open Access Journal
issn 2079-6382
language English
last_indexed 2024-03-10T19:36:13Z
publishDate 2020-05-01
publisher MDPI AG
record_format Article
series Antibiotics
spelling doaj.art-fcefc982a1cf4f9196c52d2f726875352023-11-20T01:43:53ZengMDPI AGAntibiotics2079-63822020-05-019628010.3390/antibiotics9060280Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and ExceptionsMichelle David0Clara Lejeune1Sonia Abreu2Annabelle Thibessard3Pierre Leblond4Pierre Chaminade5Marie-Joelle Virolle6Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Saclay, 91198 Gif-sur-Yvette, FranceInstitute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Saclay, 91198 Gif-sur-Yvette, FranceLipides, Systèmes Analytiques et Biologiques, Université Paris-Saclay, 92296 Châtenay-Malabry, FranceUniversité de Lorraine, INRAE, DynAMic, F-54000 Nancy, FranceUniversité de Lorraine, INRAE, DynAMic, F-54000 Nancy, FranceLipides, Systèmes Analytiques et Biologiques, Université Paris-Saclay, 92296 Châtenay-Malabry, FranceInstitute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Saclay, 91198 Gif-sur-Yvette, FranceStreptomycetes are well known antibiotic producers and are among the rare prokaryotes able to store carbon as lipids. Previous comparative studies of the weak antibiotic producer <i>Streptomyces lividans</i> with its <i>ppk</i> mutant and with <i>Streptomyces coelicolor</i>, which both produce antibiotics, suggested the existence of a negative correlation between total lipid content and the ability to produce antibiotics. To determine whether such a negative correlation can be generalized to other <i>Streptomyces</i> species, fifty-four strains were picked randomly and grown on modified R2YE medium, limited in phosphate, with glucose or glycerol as the main carbon source. The total lipid content and antibiotic activity against <i>Micrococcus luteus</i> were assessed for each strain. This study revealed that the ability to accumulate lipids was not evenly distributed among strains and that glycerol was more lipogenic than glucose and had a negative impact on antibiotic biosynthesis. Furthermore, a statistically significant negative Pearson correlation between lipid content and antibiotic activity could be established for most strains, but a few strains escape this general law. These exceptions are likely due to limits and biases linked to the type of test used to determine antibiotic activity, which relies exclusively on <i>Micrococcus luteus</i> sensitivity. They are characterized either by high lipid content and high antibiotic activity or by low lipid content and undetectable antibiotic activity against <i>Micrococcus luteus</i>. Lastly, the comparative genomic analysis of two strains with contrasting lipid content, and both named <i>Streptomyces antibioticus</i> (DSM 41,481 and DSM 40,868, which we found to be phylogenetically related to <i>Streptomyces lavenduligriseus</i>)<i>,</i> indicated that some genetic differences in various pathways related to the generation/consumption of acetylCoA could be responsible for such a difference.https://www.mdpi.com/2079-6382/9/6/280<i>Streptomyces</i>antibioticslipidstriacylglycerolmetabolismglycerol
spellingShingle Michelle David
Clara Lejeune
Sonia Abreu
Annabelle Thibessard
Pierre Leblond
Pierre Chaminade
Marie-Joelle Virolle
Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and Exceptions
Antibiotics
<i>Streptomyces</i>
antibiotics
lipids
triacylglycerol
metabolism
glycerol
title Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and Exceptions
title_full Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and Exceptions
title_fullStr Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and Exceptions
title_full_unstemmed Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and Exceptions
title_short Negative Correlation between Lipid Content and Antibiotic Activity in <i>Streptomyces</i>: General Rule and Exceptions
title_sort negative correlation between lipid content and antibiotic activity in i streptomyces i general rule and exceptions
topic <i>Streptomyces</i>
antibiotics
lipids
triacylglycerol
metabolism
glycerol
url https://www.mdpi.com/2079-6382/9/6/280
work_keys_str_mv AT michelledavid negativecorrelationbetweenlipidcontentandantibioticactivityinistreptomycesigeneralruleandexceptions
AT claralejeune negativecorrelationbetweenlipidcontentandantibioticactivityinistreptomycesigeneralruleandexceptions
AT soniaabreu negativecorrelationbetweenlipidcontentandantibioticactivityinistreptomycesigeneralruleandexceptions
AT annabellethibessard negativecorrelationbetweenlipidcontentandantibioticactivityinistreptomycesigeneralruleandexceptions
AT pierreleblond negativecorrelationbetweenlipidcontentandantibioticactivityinistreptomycesigeneralruleandexceptions
AT pierrechaminade negativecorrelationbetweenlipidcontentandantibioticactivityinistreptomycesigeneralruleandexceptions
AT mariejoellevirolle negativecorrelationbetweenlipidcontentandantibioticactivityinistreptomycesigeneralruleandexceptions