The impacts of ecological disturbances on the diversity of biosynthetic gene clusters in kauri (Agathis australis) soil

Abstract

The ancient kauri (Agathis australis) dominated forests of Aotearoa New Zealand are under threat from a multitude of ecological disturbances such as forest fragmentation, biodiversity loss, climate change, and the spread of the virulent soil pathogen Phytophthora agathidicida. Taking a wider ecosystem-level approach, our research aimed to explore the impacts of forest disturbance and disease outbreaks on the biosynthetic potential and taxonomic diversity of the kauri soil microbiome. We explored the diversity of secondary metabolite biosynthetic gene clusters (BGCs) in soils from a range of kauri forests that varied according to historical disturbance and dieback expression. To characterise the diversity of microbial BGCs, we targeted the non-ribosomal peptide synthetase (NRPS) and polyketide synthetase (PKS) gene regions for sequencing using long-read PacBio® HiFi sequencing. Furthermore, the soil bacterial and fungal communities of each forest were characterized using 16 S rRNA and ITS gene region sequencing. We identified a diverse array of naturally occurring microbial BGCs in the kauri forest soils, which may offer promising targets for the exploration of secondary metabolites with anti-microbial activity against P. agathidicida. We detected differences in the number and diversity of microbial BGCs according to forest disturbance history. Notably, soils associated with the most undisturbed kauri forest had a higher number and diversity of microbial NRPS-type BGCs, which may serve as a potential indicator of natural levels of microbiome resistance to pathogen invasion. By linking patterns in microbial biosynthetic diversity to forest disturbance history, this research highlights the need for us to consider the influence of ecological disturbances in potentially predisposing forests to disease by impacting the wider health of forest soil ecosystems. Furthermore, by identifying the range of microbial BGCs present at a naturally high abundance in kauri soils, this research contributes to the future discovery of natural microbial compounds that may potentially enhance the disease resilience of kauri forests. The methodological approaches used in this study highlight the value of moving beyond a taxonomic lens when examining the response of microbial communities to ecosystem disturbance and the need to develop more functional measures of microbial community resilience to invasive plant pathogens.