A global phenomenon of increasing bark beetle-induced tree mortality has heightened concerns regarding ecosystem response and biogeochemical implications. Here, we explore microbial dynamics under lodgepole pines through the analysis of bulk (16S rRNA gene) and potentially active (16S rRNA) communities to understand the terrestrial ecosystem responses that are associated with this form of large-scale tree mortality. We found that the relative abundances of bulk and potentially active taxa were 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 associated with the 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 the 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 bulk and potentially active communities after beetle infestation may 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 that are fueled in part by a changing climate. While aboveground processes have been explored, changes at the terrestrial interface that are 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 that rare as opposed to abundant taxa contribute disproportionately to microbial community dynamics and presumably biogeochemical cycling within these types of perturbed ecosystems.

Forested ecosystems throughout the world are experiencing increases in the incidence and magnitude of insect-induced tree mortality with large ecologic ramifications. Interestingly, correlations between water quality and the extent of tree mortality in Colorado montane ecosystems suggest compensatory effects from adjacent live vegetation that mute responses in less severely impacted forests. To this end, we investigated whether the composition of the soil bacterial community and associated functionality beneath beetle-killed lodgepole pine was influenced by the extent of surrounding tree mortality. The most pronounced changes were observed in the potentially active bacterial community, where alpha diversity increased in concert with surrounding tree mortality until mortality exceeded a tipping point of ~30 to 40%, after which diversity stabilized and decreased. Community structure also clustered in association with the extent of surrounding tree mortality with compositional trends best explained by differences in NH ₄ ⁺ concentrations and C/N ratios. C/N ratios, which were lower in soils under beetle-killed trees, further correlated with the relative abundance of putative nitrifiers and exoenzyme activity. Collectively, the response of soil microorganisms that drive heterotrophic respiration and decay supports observations of broader macroscale threshold effects on water quality in heavily infested forests and could be utilized as a predictive mechanism during analogous ecosystem disruptions. IMPORTANCE Forests around the world are succumbing to insect infestation with repercussions for local soil biogeochemistry and downstream water quality and quantity. This study utilized microbial community dynamics to address why we are observing watershed scale biogeochemical impacts from forest mortality in some impacted areas but not others. Through a unique “tree-centric” approach, we were able to delineate plots with various tree mortality levels within the same watershed to see if surviving surrounding vegetation altered microbial and biogeochemical responses. Our results suggest that forests with lower overall tree mortality levels are able to maintain “normal” ecosystem function, as the bacterial community appears resistant to tree death. However, surrounding tree mortality influences this mitigating effect with various linear and threshold responses whereupon the bacterial community and its function are altered. Our study lends insight into how microscale responses propagate upward into larger-scale observations, which may be useful for future predictions during analogous disruptions.