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. 2022 Mar 28;7(14):12171-12185.
doi: 10.1021/acsomega.2c00544. eCollection 2022 Apr 12.

Insights into the Chemical Diversity of Selected Fungi from the Tza Itzá Cenote of the Yucatan Peninsula

Carlos A Fajardo-Hernández  1 , Firoz Shah Tuglak Khan  2 , Laura Flores-Bocanegra  2 , Alejandra Prieto-Davó  3 , Baojie Wan  4 , Rui Ma  4 , Mallique Qader  4 , Rodrigo Villanueva-Silva  1 , Anahí Martínez-Cárdenas  1 , Marian A López-Lobato  1 , Shabnam Hematian  2 , Scott G Franzblau  4 , Huzefa A Raja  2 , Rodolfo García-Contreras  5 , Mario Figueroa  1
Affiliations

Insights into the Chemical Diversity of Selected Fungi from the Tza Itzá Cenote of the Yucatan Peninsula

Carlos A Fajardo-Hernández et al. ACS Omega. .

Abstract

Cenotes are habitats with unique physical, chemical, and biological features. Unexplored microorganisms from these sinkholes represent a potential source of bioactive molecules. Thus, a series of cultivable fungi (Aspergillus spp. NCA257, NCA264, and NCA276, Stachybotrys sp. NCA252, and Cladosporium sp. NCA273) isolated from the cenote Tza Itzá were subjected to chemical, coculture, and metabolomic analyses. Nineteen compounds were obtained and tested for their antimicrobial potential against ESKAPE pathogens, Mycobacterium tuberculosis, and nontuberculous mycobacteria. In particular, phenylspirodrimanes from Stachybotrys sp. NCA252 showed significant activity against MRSA, MSSA, and mycobacterial strains. On the other hand, the absolute configuration of the new compound 17-deoxy-aspergillin PZ (1) isolated from Aspergillus sp. NCA276 was established via single-crystal X-ray crystallography. Also, the chemical analysis of the cocultures between Aspergillus and Cladosporium strains revealed the production of metabolites that were not present or were barely detected in the monocultures. Finally, molecular networking analysis of the LC-MS-MS/MS data for each fungus was used as a tool for the annotation of additional compounds, increasing the chemical knowledge on the corresponding fungal strains. Overall, this is the first systematic chemical study on fungi isolated from a sinkhole in Mexico.

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Conflict of interest statement

The authors declare no competing financial interest.

Figures

Figure 1
Figure 1
Location of cenote Tza Itzá (20°43′50.27″ N, 89°27′56.82″ W) in the Yucatan peninsula.
Figure 2
Figure 2
Fungal isolates from cenote Tza Itzá on PDA medium: Aspergillus spp. NCA257, NCA264, and NCA276; Stachybotrys sp. NCA252; and Cladosporium sp. NCA273.
Figure 3
Figure 3
Isolated compounds from Aspergillus spp. NCA257, NCA264, and NCA276.
Figure 4
Figure 4
Displacement ellipsoid plot (50% probability level) of 1 at 100(2) K.
Figure 5
Figure 5
Metabolomic analysis of Aspergillus sp. NCA276. (A) FBMN (>2 nodes per cluster) and (B–E) selected clusters with nodes showing the compounds manually annotated (red circles) and by GNPS library search. Singletons (no molecular relatives) are not shown in the network.
Figure 6
Figure 6
Metabolomic analysis of Aspergillus sp. NCA264. (A) FBMN and (B,C) selected clusters with nodes showing the compounds annotated by GNPS library search.
Figure 7
Figure 7
Metabolomic analysis of Aspergillus sp. NCA257 and selected node showing manually annotated 9 (red circle).
Figure 8
Figure 8
Isolated compounds from Stachybotrys sp. NCA252.
Figure 9
Figure 9
Metabolomic analysis of Stachybotrys sp. NCA252. (A) FBMN and (B–F) selected clusters with nodes showing the compounds manually annotated (red circles) and by GNPS library search.
Figure 10
Figure 10
Fungal interaction between Aspergillus spp. NCA257 and NCA276 and Cladosporium sp. NCA273 in PDA plates.
Figure 11
Figure 11
HPLC traces (PDA UV λ = 254 nm) of monoculture extracts of Aspergillus sp. NCA257 and Cladosporium sp. NCA273 and the coculture extract.
Figure 12
Figure 12
HPLC traces (PDA UV λ = 254 nm) of monoculture extracts of Aspergillus spp. NCA257 and NCA276 and the coculture extract.
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