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Aspergillus flavus grown in peptone as the carbon source exhibits spore density- and peptone concentration-dependent aflatoxin biosynthesis.

Yan S, Liang Y, Zhang J, Liu CM - BMC Microbiol. (2012)

Bottom Line: Metabolomic studies revealed that, in addition to inhibited AF biosynthesis, mycelia grown in peptone media with a high initial spore density showed suppressed fatty acid biosynthesis, reduced tricarboxylic acid (TCA) cycle intermediates, and increased pentose phosphate pathway products.Additions of TCA cycle intermediates had no effect on AF biosynthesis, suggesting the inhibited AF biosynthesis was not caused by depleted TCA cycle intermediates.This switching ability may offer Aspergillus species a competition advantage in natural ecosystems, producing AFs only when self-population is low and food is scarce.

View Article: PubMed Central - HTML - PubMed

Affiliation: Practaculture College, Gansu Agricultural University, Lanzhou 730070, China.

ABSTRACT

Background: Aflatoxins (AFs) are highly carcinogenic compounds produced by Aspergillus species in seeds with high lipid and protein contents. It has been known for over 30 years that peptone is not conducive for AF productions, although reasons for this remain unknown.

Results: In this study, we showed that when Aspergillus flavus was grown in peptone-containing media, higher initial spore densities inhibited AF biosynthesis, but promoted mycelial growth; while in glucose-containing media, more AFs were produced when initial spore densities were increased. This phenomenon was also observed in other AF-producing strains including A. parasiticus and A. nomius. Higher peptone concentrations led to inhibited AF production, even in culture with a low spore density. High peptone concentrations did however promote mycelial growth. Spent medium experiments showed that the inhibited AF production in peptone media was regulated in a cell-autonomous manner. mRNA expression analyses showed that both regulatory and AF biosynthesis genes were repressed in mycelia cultured with high initial spore densities. Metabolomic studies revealed that, in addition to inhibited AF biosynthesis, mycelia grown in peptone media with a high initial spore density showed suppressed fatty acid biosynthesis, reduced tricarboxylic acid (TCA) cycle intermediates, and increased pentose phosphate pathway products. Additions of TCA cycle intermediates had no effect on AF biosynthesis, suggesting the inhibited AF biosynthesis was not caused by depleted TCA cycle intermediates.

Conclusions: We here demonstrate that Aspergillus species grown in media with peptone as the sole carbon source are able to sense their own population densities and peptone concentrations to switch between rapid growth and AF production. This switching ability may offer Aspergillus species a competition advantage in natural ecosystems, producing AFs only when self-population is low and food is scarce.

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The density effect is present in allAspergillusstrains tested exceptA. flavusNRRL 3357. Strains of A. flavus NRRL 3357, A. parasiticus NRRL 2999 and A. nomius NRRL 13137 were tested for their density effects. Freshly prepared spores at the densities of 102 to 106 were cultured in GMS and PMS media and AF contents were analyzed by TLC after 3 days. Note no AF was produced in PMS media by A. flavus NRRL 3357. St: AF standards.
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Figure 5: The density effect is present in allAspergillusstrains tested exceptA. flavusNRRL 3357. Strains of A. flavus NRRL 3357, A. parasiticus NRRL 2999 and A. nomius NRRL 13137 were tested for their density effects. Freshly prepared spores at the densities of 102 to 106 were cultured in GMS and PMS media and AF contents were analyzed by TLC after 3 days. Note no AF was produced in PMS media by A. flavus NRRL 3357. St: AF standards.

Mentions: To elucidate if the density effect is a general phenomenon in AF-producing strains, we obtained A. flavus NRRL 3357, A. parasiticus NRRL 2999 and A. nomius NRRL 13137 from the Agricultural Research Service (ARS) culture collection in United States Department of Agriculture (USDA), and performed experiments in parallel with A. flavus A3.2890. Fresh spore suspensions were prepared in the same way as for A. flavus A3.2890, and inoculated in PMS or GMS liquid media with initial spore densities from 102 spores/ml to 106 spores/ml. After three-day cultures, AFs were extracted from media and analyzed by TLC. As shown in Figure 5, in GMS media, all strains showed increased AF productions when initial spore densities were increased from 102 to 106 spores/ml, excluding A. flavus NRRL 3357. As reported previously, only AFB1 and AFB2 were produced by A. flavus NRRL 3357 [48], while for all other strains AFB1 and AFG1 were the major AFs produced.


Aspergillus flavus grown in peptone as the carbon source exhibits spore density- and peptone concentration-dependent aflatoxin biosynthesis.

Yan S, Liang Y, Zhang J, Liu CM - BMC Microbiol. (2012)

The density effect is present in allAspergillusstrains tested exceptA. flavusNRRL 3357. Strains of A. flavus NRRL 3357, A. parasiticus NRRL 2999 and A. nomius NRRL 13137 were tested for their density effects. Freshly prepared spores at the densities of 102 to 106 were cultured in GMS and PMS media and AF contents were analyzed by TLC after 3 days. Note no AF was produced in PMS media by A. flavus NRRL 3357. St: AF standards.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3412747&req=5

Figure 5: The density effect is present in allAspergillusstrains tested exceptA. flavusNRRL 3357. Strains of A. flavus NRRL 3357, A. parasiticus NRRL 2999 and A. nomius NRRL 13137 were tested for their density effects. Freshly prepared spores at the densities of 102 to 106 were cultured in GMS and PMS media and AF contents were analyzed by TLC after 3 days. Note no AF was produced in PMS media by A. flavus NRRL 3357. St: AF standards.
Mentions: To elucidate if the density effect is a general phenomenon in AF-producing strains, we obtained A. flavus NRRL 3357, A. parasiticus NRRL 2999 and A. nomius NRRL 13137 from the Agricultural Research Service (ARS) culture collection in United States Department of Agriculture (USDA), and performed experiments in parallel with A. flavus A3.2890. Fresh spore suspensions were prepared in the same way as for A. flavus A3.2890, and inoculated in PMS or GMS liquid media with initial spore densities from 102 spores/ml to 106 spores/ml. After three-day cultures, AFs were extracted from media and analyzed by TLC. As shown in Figure 5, in GMS media, all strains showed increased AF productions when initial spore densities were increased from 102 to 106 spores/ml, excluding A. flavus NRRL 3357. As reported previously, only AFB1 and AFB2 were produced by A. flavus NRRL 3357 [48], while for all other strains AFB1 and AFG1 were the major AFs produced.

Bottom Line: Metabolomic studies revealed that, in addition to inhibited AF biosynthesis, mycelia grown in peptone media with a high initial spore density showed suppressed fatty acid biosynthesis, reduced tricarboxylic acid (TCA) cycle intermediates, and increased pentose phosphate pathway products.Additions of TCA cycle intermediates had no effect on AF biosynthesis, suggesting the inhibited AF biosynthesis was not caused by depleted TCA cycle intermediates.This switching ability may offer Aspergillus species a competition advantage in natural ecosystems, producing AFs only when self-population is low and food is scarce.

View Article: PubMed Central - HTML - PubMed

Affiliation: Practaculture College, Gansu Agricultural University, Lanzhou 730070, China.

ABSTRACT

Background: Aflatoxins (AFs) are highly carcinogenic compounds produced by Aspergillus species in seeds with high lipid and protein contents. It has been known for over 30 years that peptone is not conducive for AF productions, although reasons for this remain unknown.

Results: In this study, we showed that when Aspergillus flavus was grown in peptone-containing media, higher initial spore densities inhibited AF biosynthesis, but promoted mycelial growth; while in glucose-containing media, more AFs were produced when initial spore densities were increased. This phenomenon was also observed in other AF-producing strains including A. parasiticus and A. nomius. Higher peptone concentrations led to inhibited AF production, even in culture with a low spore density. High peptone concentrations did however promote mycelial growth. Spent medium experiments showed that the inhibited AF production in peptone media was regulated in a cell-autonomous manner. mRNA expression analyses showed that both regulatory and AF biosynthesis genes were repressed in mycelia cultured with high initial spore densities. Metabolomic studies revealed that, in addition to inhibited AF biosynthesis, mycelia grown in peptone media with a high initial spore density showed suppressed fatty acid biosynthesis, reduced tricarboxylic acid (TCA) cycle intermediates, and increased pentose phosphate pathway products. Additions of TCA cycle intermediates had no effect on AF biosynthesis, suggesting the inhibited AF biosynthesis was not caused by depleted TCA cycle intermediates.

Conclusions: We here demonstrate that Aspergillus species grown in media with peptone as the sole carbon source are able to sense their own population densities and peptone concentrations to switch between rapid growth and AF production. This switching ability may offer Aspergillus species a competition advantage in natural ecosystems, producing AFs only when self-population is low and food is scarce.

Show MeSH