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 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. IMPORTANCEForests 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.

Vertical vs. horizontal transmission of the microbiome in a key disease vector, Ixodes pacificus

“…However, the non‐ Rickettsia component of the tick microbiome may be more important to overall diversity patterns associated with pathogen transmission dynamics. Rare taxa in the microbiome may play a disproportionally important role in community structure and response to disturbance (Mikkelson, Bokman, & Sharp, ; Shade et al., ). To examine the components of the tick microbiome that may be obscured by the dominant endosymbiont, we computationally removed Rickettsia sequence reads from nymphal I. pacificus ticks.…”

Changes of Scots Pine Phyllosphere and Soil Fungal Communities during Outbreaks of Defoliating Insects

“…In addition, the extent of infestation was found to determine the biogeochemical responses as well as the soil bacterial communities [33,35]. Mikkelson et al [34] elegantly highlighted the importance of rare bacterial taxa on the community dynamics and presumably biogeochemical cycling under bark beetle-induced tree mortality. Because DGGE visualizes only amplicons originating from dominant species, the effect of defoliation on rare taxa might have remained undetected, although they might be critical in maintaining ecosystem functioning.…”

“…The effects of outbreaks of single pests either on phyllosphere or soil microbial communities have been studied already (e.g., [21,24,[27][28][29][30][31][32][33][34][35]), but these data did not simultaneously compare the effect of pest outbreaks on phyllosphere and soil microbial communities and did not differentiate between the effects of different pest insects in the same forest ecosystem. Here, we analyzed the effect of outbreaks of two defoliating insects, nun moth or pine tree lappet, in Scots pine stands in eastern Germany on the bacterial and fungal community structure in the soil and the phyllosphere using DGGE.…”

Ecosystem Resilience and Limitations Revealed by Soil Bacterial Community Dynamics in a Bark Beetle-Impacted Forest

“…Fungal communities have shown extensive changes after beetle-induced tree mortality, with decreases in fungi associated symbiotically with tree roots coupled with increases in saprotrophic fungi ( 19 ). Surprisingly, studies have not reported a similar magnitude of response of the bacterial community after insect infestation, as observations have varied in magnitude ( 7 , 9 , 19 , 20 ). This suggests that the local bacterial soil community within these perturbed forests might have an inherent level of resilience to this type of ecosystem disruption.…”

“…While studies have investigated how the microbial community changes beneath beetle-killed trees ( 7 , 9 , 19 , 20 ), little is understood about why the magnitude of these changes differs between studies. Recently, it has been determined that a certain threshold of localized tree mortality must be attained before observable changes in soil carbon and nitrogen pools and respiration rates beneath beetle-killed lodgepole pine trees occur ( 21 ), presumably because adjacent live trees exert a compensatory effect following a forest disturbance.…”