Altered edaphic parameters couple to shifts in terrestrial bacterial community structure associated with insect-induced tree mortality

Abstract

Unprecedented insect-induced tree mortality has been observed globally and while hydrologic and biogeochemical changes have been recorded, alterations to terrestrial microbial communities, which influence as well as respond to these shifts, are not well understood. The objective of this work was to better understand how bacterial communities are coupled to perturbations in biogeochemically-relevant soil physicochemical parameters resulting from beetle-induced tree death. To this end, soils beneath trees across a beetle-kill spectrum were contrasted in the central Rocky Mountains at both heavily impacted (Chimney, 85% mortality) and moderately impacted (Niwot, 18% mortality) field sites. Soil organic matter (OM), dissolved organic carbon (DOC) and dissolved organic nitrogen were all significantly altered when contrasting soils under healthy versus beetle-attacked trees at Chimney. Bacterial alpha diversity measurements were found to increase with tree death and beta diversity measures showed significant clustering with relation to tree phase. The site was characterized by a significantly higher relative abundance of bacterial clades under healthy trees that were correlated to OM and DOC concentrations. In contrast, compositional changes in soil bacterial communities and edaphic parameters associated with tree phase were not observed at the less impacted Niwot site. Our findings reveal a coupled response between shifts in organic carbon cycling and the bacterial assemblage as a result of large-scale, beetle-induced tree mortality with implications for heterotrophic respiration in near-surface soils and suggests a possible dependence on the level of forest mortality before manifestation.

Rare Taxa Maintain Microbial Diversity and Contribute to Terrestrial Community Dynamics throughout Bark Beetle Infestation

“…However, we not only observed differences in the structures of bacterial communities associated with the metabolically active versus bulk fractions, which have been recorded previously in unperturbed forest ecosystems (22), but they further clustered into fractions that were associated with various stages of tree mortality. This is in opposition to two previous studies at the site (11,12) that discerned no significant differences in bulk bacterial community structures under green-, red-, or grayphase trees. This discrepancy may be explained by a hysteresis effect occurring at Niwot Ridge, in which observable changes to bacterial community structure lag several years behind tree mortality.…”

“…This discrepancy may be explained by a hysteresis effect occurring at Niwot Ridge, in which observable changes to bacterial community structure lag several years behind tree mortality. Mikkelson et al (12) sampled under lodgepole pine trees 1 year prior to the present study, and Ferrenberg et al (11) sampled under limber pine trees 3 years prior. It is also possible that these contradictory results are due to the sampling of different tree species or intra-annual climatic and sampling variability.…”

“…Niwot Ridge is located in the Rocky Mountains, with an elevation of approximately 2,800 m, a mean annual air temperature of 1 to 3°C, and precipitation of around 800 mm/year. Additional site characteristics can be found in Xiong et al (23) and Mikkelson et al (12). The same three "green-phase" trees, three "red-phase" trees, and three "gray-phase" trees were sampled at each event (n ϭ 9 for each sampling event, and n ϭ 27 for the sampling season).…”

“…Subsequently, each soil sample was analyzed for pH, water content (WC), organic matter content (OM), total nitrogen (TN), and dissolved organic carbon (DOC) after sieving down to 2 mm as detailed in Mikkelson et al (12). DNA/RNA extraction and preparation.…”

“…Two studies reported limited changes to soil bacteria after the insect-induced mortality of spruce (10) and limber pines (11), which suggests that these bacterial communities are more resistant to perturbation. However, a subsequent study documented a significant bacterial response coupled with altered edaphic parameters in soils within a forest that was heavily impacted by beetles (ϳ85% mortality) and suggested that there may be a threshold level of mortality necessary to observe a bacterial response within these systems (12). While forest response to more traditionally studied disturbances, such as harvesting, windfall, and fire, differs from that of beetle kill (13), past research into forest harvesting has found that there is a threshold level of tree clearing necessary before observing changes to local soil biogeochemistry (14,15).…”