Shedding light on Aspergillus niger volatile exometabolome

Costa, Carina Pedrosa; Silva, Diogo G; Rudnitskaya, Alisa; Almeida, Adelaide; Rocha, Sı́lvia M.

doi:10.1038/srep27441

Cited by 37 publications

(51 citation statements)

References 47 publications

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“…To the best of our knowledge, none of the reported molecules have previously been measured in the headspace of A. fumigatus cultures, likely because the hypoxia-associated volatile metabolome of this organism has never been measured. Five of the six molecules (excluding benzonitrile) have, however, been measured in the headspace of either Aspergillus flavus or Aspergillus niger cultures [35, 36]. …”

Section: Resultsmentioning

confidence: 99%

Sniffing out the hypoxia volatile metabolic signature ofAspergillus fumigatus

et al. 2017

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Invasive Aspergillosis (IA) is a life-threatening infectious disease caused by fungi from the genus Aspergillus, with an associated mortality as high as 90% in certain populations. IA-associated pulmonary lesions are characteristically depleted in oxygen relative to normal lung tissue, and it has been shown that the most common causal agent of IA, Aspergillus fumigatus, must respond to low-oxygen environments for pathogenesis and disease progression. Previous studies have demonstrated marked alterations to the Aspergillus fumigatus transcriptome in response to low oxygen environments that induce a “hypoxia response.” Consequently, we hypothesized that these transcriptomic changes would alter the volatile metabolome and generate a volatile hypoxia signature. In the present study, we analyzed the volatile molecules produced by A. fumigatus in both oxygen replete (normoxia) and depleted (hypoxia) environments via headspace solid-phase microextraction coupled to two-dimensional gas chromatography-time-of-flight mass spectrometry (HS-SPME-GC×GC-TOFMS). Using the machine learning algorithm Random Forest, we identified 19 volatile molecules that were discriminatory between the four growth conditions assessed in this study (i.e., early hypoxia (1 h), late hypoxia (8 h), early normoxia (1 h), and late normoxia (8 h)), as well as a set of 19 that were discriminatory between late hypoxia cultures and all other growth conditions in aggregate. Nine molecules were common to both comparisons, while the remaining 20 were specific to only one of two. We assigned putative identifications to 13 molecules, of which six were most highly abundant in late hypoxia cultures. Previously acquired transcriptomic data identified putative biochemical pathways induced in hypoxia conditions that plausibly account for the production of a subset of these molecules, including 2,3-butanedione and 3-hydroxy-2-butanone. These two molecules may represent a novel hypoxia fitness pathway in A. fumigatus, and could be useful in the detection of hypoxia-associated A. fumigatus lesions that develop in established IA infections.

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Section: Resultsmentioning

confidence: 99%

Sniffing out the hypoxia volatile metabolic signature ofAspergillus fumigatus

et al. 2017

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“…Aspergillus niger has been claimed to produce a very large number of secondary metabolites (Table 6 ; Nielsen et al 2009 ) including isoflavones which are actually plant metabolites (Umezawa et al 1975 ; Nielsen et al 2009 ). Apart from many volatiles and small organic acids (Wani et al 2010 ; Priegnitz et al 2015 ; Costa et al 2016 ), A. niger sensu stricto can produce a variety of other secondary metabolites. In many cases, fungi identified as A. niger were indeed A. tubingensis or other closely related species (Table 2 ).…”

Section: Secondary Metabolite Potentialmentioning

confidence: 99%

Safety of the fungal workhorses of industrial biotechnology: update on the mycotoxin and secondary metabolite potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei

Frisvad

Møller

Larsen

et al. 2018

Appl Microbiol Biotechnol

256

269

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This review presents an update on the current knowledge of the secondary metabolite potential of the major fungal species used in industrial biotechnology, i.e., Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei. These species have a long history of safe use for enzyme production. Like most microorganisms that exist in a challenging environment in nature, these fungi can produce a large variety and number of secondary metabolites. Many of these compounds present several properties that make them attractive for different industrial and medical applications. A description of all known secondary metabolites produced by these species is presented here. Mycotoxins are a very limited group of secondary metabolites that can be produced by fungi and that pose health hazards in humans and other vertebrates when ingested in small amounts. Some mycotoxins are species-specific. Here, we present scientific basis for (1) the definition of mycotoxins including an update on their toxicity and (2) the clarity on misclassification of species and their mycotoxin potential reported in literature, e.g., A. oryzae has been wrongly reported as an aflatoxin producer, due to misclassification of Aspergillus flavus strains. It is therefore of paramount importance to accurately describe the mycotoxins that can potentially be produced by a fungal species that is to be used as a production organism and to ensure that production strains are not capable of producing mycotoxins during enzyme production. This review is intended as a reference paper for authorities, companies, and researchers dealing with secondary metabolite assessment, risk evaluation for food or feed enzyme production, or considerations on the use of these species as production hosts.

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“…The samples extraction methods for VOCs analysis was performed using the methods adapted from Costa et al ( 2016 ). The fungal biomass (3 biological replicates) for A. oryzae RIB 40 (S1: KACC 44967) S1 VMI and S1 were harvested at stipulated time point by adding Ringer's solution (10 mL/per plate).…”

Section: Methodsmentioning

confidence: 99%

Volatiles Mediated Interactions Between Aspergillus oryzae Strains Modulate Morphological Transition and Exometabolomes

Singh

Lee

2018

Front. Microbiol.

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Notwithstanding its mitosporic nature, an improbable morpho-transformation state i. e., sclerotial development (SD), is vaguely known in Aspergillus oryzae. Nevertheless an intriguing phenomenon governing mold's development and stress response, the effects of exogenous factors engendering SD, especially the volatile organic compounds (VOCs) mediated interactions (VMI) pervasive in microbial niches have largely remained unexplored. Herein, we examined the effects of intra-species VMI on SD in A. oryzae RIB 40, followed by comprehensive analyses of associated growth rates, pH alterations, biochemical phenotypes, and exometabolomes. We cultivated A. oryzae RIB 40 (S1VMI: KACC 44967) opposite a non-SD partner strain, A. oryzae (S2: KCCM 60345), conditioning VMI in a specially designed “twin plate assembly.” Notably, SD in S1VMI was delayed relative to its non-conditioned control (S1) cultivated without partner strain (S2) in twin plate. Selectively evaluating A. oryzae RIB 40 (S1VMI vs. S1) for altered phenotypes concomitant to SD, we observed a marked disparity for corresponding growth rates (S1VMI < S1)7days, media pH (S1VMI > S1)7days, and biochemical characteristics viz., protease (S1VMI > S1)7days, amylase (S1VMI > nS1)3–7days, and antioxidants (S1VMI > S1)7days levels. The partial least squares—discriminant analysis (PLS-DA) of gas chromatography—time of flight—mass spectrometry (GC-TOF-MS) datasets for primary metabolites exhibited a clustered pattern (PLS1, 22.04%; PLS2, 11.36%), with 7 days incubated S1VMI extracts showed higher abundance of amino acids, sugars, and sugar alcohols with lower organic acids and fatty acids levels, relative to S1. Intriguingly, the higher amino acid and sugar alcohol levels were positively correlated with antioxidant activity, likely impeding SD in S1VMI. Further, the PLS-DA (PLS1, 18.11%; PLS2, 15.02%) based on liquid chromatography—mass spectrometry (LC-MS) datasets exhibited a notable disparity for post-SD (9–11 days) sample extracts with higher oxylipins and 13-desoxypaxilline levels in S1VMI relative to S1, intertwining Aspergillus morphogenesis and secondary metabolism. The analysis of VOCs for the 7 days incubated samples displayed considerably higher accumulation of C-8 compounds in the headspace of twin-plate experimental sets (S1VMI:S2) compared to those in non-conditioned controls (S1 and S2—without respective partner strains), potentially triggering altered morpho-transformation and concurring biochemical as well as metabolic states in molds.

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Shedding light on Aspergillus niger volatile exometabolome

Cited by 37 publications

References 47 publications

Sniffing out the hypoxia volatile metabolic signature ofAspergillus fumigatus

Sniffing out the hypoxia volatile metabolic signature ofAspergillus fumigatus

Safety of the fungal workhorses of industrial biotechnology: update on the mycotoxin and secondary metabolite potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei

Volatiles Mediated Interactions Between Aspergillus oryzae Strains Modulate Morphological Transition and Exometabolomes

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