Metabolomic Analysis of Aspergillus niger Isolated From the International Space Station Reveals Enhanced Production Levels of the Antioxidant Pyranonigrin A

Abstract

Secondary metabolite (SM) production in Aspergillus niger JSC-093350089, isolated from the International Space Station (ISS), is reported, along with a comparison to the experimentally established strain ATCC 1015. The analysis revealed enhanced production levels of naphtho-γ-pyrones and therapeutically relevant SMs, including bicoumanigrin A, aurasperones A and B, and the antioxidant pyranonigrin A. Genetic variants that may be responsible for increased SM production levels in JSC-093350089 were identified. These findings include INDELs within the predicted promoter region of flbA , which encodes a developmental regulator that modulates pyranonigrin A production via regulation of Fum21. The pyranonigrin A biosynthetic gene cluster was confirmed in A. niger , which revealed the involvement of a previously undescribed gene, pyrE , in its biosynthesis. UVC sensitivity assays enabled characterization of pyranonigrin A as a UV resistance agent in the ISS isolate.

Advances in space microbiology

“…In another study, Aspergillus nidulans nkuA mutant exposed to spaceflight conditions resulted in significant production of asperthicin, an anthraquinone pigment ( Romsdahl et al., 2019 ). Aspergillus niger strain isolated from the ISS exhibited a 6,000% increase in the production of an antioxidant pyranonigrin, compared with the reference strain ATCC 1015 ( Romsdahl et al., 2020 ). Genomic analysis indicated the presence of INDELs within the promoter of flbA , a regulator of pyranonigrin production that might contribute to its enhanced production ( Aerts et al., 2018 ).…”

Microbial Pathogenicity in Space

“…It is now known that many microorganisms survive in our atmosphere, with reports of maintenance of viability of pathogenic strains after exposure to the stratosphere [ 8 , 13 ]. Microbial isolations have been successfully performed from air and dust samples from the troposphere and stratosphere [ 8 ], and many others have been made from space station such as those described in [ 14 , 15 , 16 , 17 , 18 ].…”

“…A few of them adapt to the unique stresses they encounter, by changing some of their phenotypical characteristics to try to gain some selective advantage. An example of this is seen for fungi and their production of secondary metabolites [ 18 ].…”

“…This species, highly relevant for its biotechnological applications, has been reported as an opportunistic human pathogen [ 84 ]. Romsdahl et al [ 18 ] isolated this species from ISS surfaces, and after extensive analysis found it to have a different secondary metabolite profile. It presented an increased production of pyranonigrin A, a molecule with antioxidant and UV-protective properties, which could explain the resistance of this strain to the ISS environment conditions [ 18 ].…”

“…Many studies [ 15 , 16 , 18 , 55 , 79 ] were performed on the survival, development and adaptation of fungal species to outer space environments; some researched fungal contamination of different surfaces in space environments such as the Mir station or the ISS [ 70 , 85 ], with a few even suggesting the need for technological development of new types of material with antimicrobial properties, so as to avoid contamination by fungi [ 85 ] and other microorganisms [ 86 ]. Part of these efforts are driven by the detrimental effect that fungal growth and activity has on equipment and materials at the ISS.…”