Rare taxa maintain microbial diversity and contribute to terrestrial community dynamics throughout bark beetle infestation

Abstract

A global phenomenon of increasing bark beetle-induced tree mortality has heightened concern regarding ecosystem response and biogeochemical implications. Here we explore microbial dynamics under lodgepole pines through the analysis of bulk (16S rDNA) and potentially active (16S rRNA) communities to understand terrestrial ecosystem responses associated with this form of large-scale tree morality. We found that the relative abundance of bulk and potentially active taxa was correlated across taxonomic levels, but at lower levels cladal differences became more apparent. Despite this correlation, there was a strong differentiation of community composition between bulk and potentially active taxa, with further clustering in association with stages of tree mortality. Surprisingly, community clustering as a function of tree phase had limited correlation to soil water content and total nitrogen concentrations, which were the only two measured edaphic parameters to differ in association with tree phase. Bacterial clustering is more readily explained by the observed decrease in abundance of active, rare microorganisms after tree death in conjunction with stable alpha diversity measurements. This enables the rare fraction of the terrestrial microbial community to maintain metabolic diversity by transitioning between metabolically active and dormant states during this ecosystem disturbance and contributes disproportionately to community dynamics and archived metabolic capabilities. These results suggest that analyzing the bulk and potentially active communities after beetle infestation might be a more sensitive indicator of disruption than measuring local edaphic parameters.

Importance: Forests around the world are experiencing unprecedented mortality due to insect infestations fueled in part by a changing climate. While above-ground processes have been explored, changes at the terrestrial interface relevant to microbial biogeochemical cycling remain largely unknown. In this study, we investigated the changing bulk and potentially active microbial communities beneath healthy and beetle-killed trees. We found that even though few edaphic parameters were altered from beetle infestation, the rare microbes were more likely to be active and fluctuate between dormancy and metabolic activity. This indicates rare as opposed to abundant taxa contribute disproportionately to microbial community dynamics and presumably biogeochemical cycling within these types of perturbed ecosystems.