Exploring the biosynthesis potential of permafrost microbiomes.

Background: Permafrost microbiomes are of paramount importance for the biogeochemistry of high latitude soils and while endemic biosynthetic domain sequences involved in secondary metabolism have been found in polar surface soils, the biosynthetic potential of permafrost microbiomes remains unexplored. Moreover, the nature of these ecosystems facilitates the unique opportunity to study the distribution and diversity of biosynthetic genes in relic DNA from ancient microbiomes. To explore the biosynthesis potential in permafrost, we used adenylation (AD) domain sequencing to evaluate non-ribosomal peptide (NRP) production in permafrost cores housing microbiomes separated at kilometer and kiloyear scales.

Results: Permafrost microbiomes represented NRP repertoires significantly different from that of temperate soil microbiomes, but as for temperate soils, the estimated domain richness and diversity was strongly correlated to the bacterial taxonomic diversity across locations. Furthermore, we found significant differences in both community composition and AD domain composition across geographical and temporal distances. Overall, the vast majority of biosynthetic domains showed below 90% amino acid similarity to characterized BGCs, confirming the high degree of novelty of NRPs inherent to permafrost microbiomes. Using available metagenomic sequences, we further identified a high biosynthetic diversity beyond NRPs throughout arctic surface soils down to deep and ancient (megayear old) permafrost microbiomes.

Conclusion: We have shown that arctic permafrost microbiomes harbor a unique biosynthetic repertoire rich in hitherto undescribed NRPs. This diversity is driven by geographic separation across kilometer scales and by the bacterial taxonomic diversity between microbiomes confined in separate permafrost layers. Hence the permafrost biome represents a unique resource for studying secondary metabolism, and potentially for the discovery of novel drug leads.