Sloth hair as a novel source of fungi with potent anti-parasitic, anti-cancer and anti-bacterial bioactivity

Abstract

The extraordinary biological diversity of tropical forests harbors a rich chemical diversity with enormous potential as a source of novel bioactive compounds. Of particular interest are new environments for microbial discovery. Sloths--arboreal mammals commonly found in the lowland forests of Panama--carry a wide variety of micro- and macro-organisms on their coarse outer hair. Here we report for the first time the isolation of diverse and bioactive strains of fungi from sloth hair, and their taxonomic placement. Eighty-four isolates of fungi were obtained in culture from the surface of hair that was collected from living three-toed sloths (Bradypus variegatus, Bradypodidae) in Soberanía National Park, Republic of Panama. Phylogenetic analyses revealed a diverse group of Ascomycota belonging to 28 distinct operational taxonomic units (OTUs), several of which are divergent from previously known taxa. Seventy-four isolates were cultivated in liquid broth and crude extracts were tested for bioactivity in vitro. We found a broad range of activities against strains of the parasites that cause malaria (Plasmodium falciparum) and Chagas disease (Trypanosoma cruzi), and against the human breast cancer cell line MCF-7. Fifty fungal extracts were tested for antibacterial activity in a new antibiotic profile screen called BioMAP; of these, 20 were active against at least one bacterial strain, and one had an unusual pattern of bioactivity against Gram-negative bacteria that suggests a potentially new mode of action. Together our results reveal the importance of exploring novel environments for bioactive fungi, and demonstrate for the first time the taxonomic composition and bioactivity of fungi from sloth hair.

Figure 1. Results of maximum likelihood and Bayesian analyses of ITSrDNA data for fungi isolated in culture from coarse, outer hair of three-toed sloths in Soberanía National Park, Panama.

Topology of each tree reflects ML analysis, and values above branches indicate ML bootstrap values and Bayesian posterior probabilities (>0.50 and >0.75, respectively). Outgroups and taxon sampling for each tree were validated by literature surveys (see methods). Taxonomic conclusions are presented in Table 1. Figure 1(A): Placement of F5073 in group 17; (B) F4847 in group 18; (C) F4831a in group 19; (D) F4819 in group 20; (E) F4801 in group 5; (F) F4806 in group 7; (G) F4886 in group 8; (H) F5071 in group 15; (I) F4812–F4816, F4830, F4831, F4845, F4852–F4856, F4860, F4873, F4882, F4883 and F4900–F4902 in group 1; (J) F4803, F4817, F4820, F4823, F4824, F4826, F4827, F4829, F4837, F4841, F4842, F4846, F4848, F4857, F4858, F4861, F4862, F4870, F4872, F4875, F4878, F4879, F4894–F4896, F4908, F4909, F5069 and F5074 in group 2; (K) F4818 and F4839 in group 10; (L) F4877, F4890 and F4897 in group 11; (M) F4828 and F4898 in group 12; (N) F4876 and F4881 in group 13; (O) F4863 and F4884 in group 6; (P) F4821, F4874, F4889 and F4913 in group 3; (Q) F4802, F4807, F4825, F4844, F4906 and F5068 in group 4; (R) F4850 and F4891 in group 9; (S) F4904 and F4905 in group 14; and (T) F5070 and F5072 in group 16.