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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.

SUBMITTER: Mikkelson KM

PROVIDER: S-EPMC5103090 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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

Mikkelson Kristin M KM Bokman Chelsea C Sharp Jonathan O JO

Applied and environmental microbiology 20160916 23

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 taxono ...[more]

PMID: 27637881

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Project description:Microbial communities typically contain many rare taxa that make up the majority of the observed membership, yet the contribution of this microbial "rare biosphere" to community dynamics is unclear. Using 16S rRNA amplicon sequencing of 3,237 samples from 42 time series of microbial communities from nine different ecosystems (air; marine; lake; stream; adult human skin, tongue, and gut; infant gut; and brewery wastewater treatment), we introduce a new method to detect typically rare microbial taxa that occasionally become very abundant (conditionally rare taxa [CRT]) and then quantify their contributions to temporal shifts in community structure. We discovered that CRT made up 1.5 to 28% of the community membership, represented a broad diversity of bacterial and archaeal lineages, and explained large amounts of temporal community dissimilarity (i.e., up to 97% of Bray-Curtis dissimilarity). Most of the CRT were detected at multiple time points, though we also identified "one-hit wonder" CRT that were observed at only one time point. Using a case study from a temperate lake, we gained additional insights into the ecology of CRT by comparing routine community time series to large disturbance events. Our results reveal that many rare taxa contribute a greater amount to microbial community dynamics than is apparent from their low proportional abundances. This observation was true across a wide range of ecosystems, indicating that these rare taxa are essential for understanding community changes over time. Importance: Microbial communities and their processes are the foundations of ecosystems. The ecological roles of rare microorganisms are largely unknown, but it is thought that they contribute to community stability by acting as a reservoir that can rapidly respond to environmental changes. We investigated the occurrence of typically rare taxa that very occasionally become more prominent in their communities ("conditionally rare"). We quantified conditionally rare taxa in time series from a wide variety of ecosystems and discovered that not only were conditionally rare taxa present in all of the examples, but they also contributed disproportionately to temporal changes in diversity when they were most abundant. This result indicates an important and general role for rare microbial taxa within their communities.

Project description:Bark beetle outbreaks have intensified in many forests around the globe in recent years. Yet, the legacy of these disturbances for future forest development remains unclear. Bark beetle disturbances are expected to increase further because of climate change. Consequently, feedbacks within the disturbance regime are of growing interest, for example, whether bark beetle outbreaks are amplifying future bark beetle activity (through the initiation of an even-aged cohort of trees) or dampening it (through increased structural and compositional diversity).We studied bark beetle-vegetation-climate interactions in the Bavarian Forest National Park (Germany), an area characterised by unprecedented bark beetle activity in the recent past. We simulated the effect of future bark beetle outbreaks on forest structure and composition and analysed how disturbance-mediated forest dynamics influence future bark beetle activity under different scenarios of climate change. We used process-based simulation modelling in combination with machine learning to disentangle the long-term interactions between vegetation, climate and bark beetles at the landscape scale.Disturbances by the European spruce bark beetle were strongly amplified by climate change, increasing between 59% and 221% compared to reference climate. Bark beetle outbreaks reduced the dominance of Norway spruce (Picea abies (L.) Karst.) on the landscape, increasing compositional diversity. Disturbances decreased structural diversity within stands (α diversity) and increased structural diversity between stands (β diversity). Overall, disturbance-mediated changes in forest structure and composition dampened future disturbance activity (a reduction of up to -67%), but were not able to fully compensate for the amplifying effect of climate change. Synthesis. Our findings indicate that the recent disturbance episode at the Bavarian Forest National Park was caused by a convergence of highly susceptible forest structures with climatic conditions favourable for bark beetle outbreaks. While future climate is increasingly conducive to massive outbreaks, the emerging landscape structure is less and less likely to support them. This study improves our understanding of the long-term legacies of ongoing bark beetle disturbances in Central Europe. It indicates that increased diversity provides an important dampening feedback, and suggests that preventing disturbances or homogenizing post-disturbance forests could elevate the future susceptibility to large-scale bark beetle outbreaks.

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Project description:Long distance dispersal to locate suitable breeding sites is recognized as a key trait influencing the population dynamics and distribution of bark beetles and other saprophytic insects. While dispersal behavior has been studied for a range of aggressive 'tree killing' bark beetles, few have considered the dispersal behaviour of non-aggressive saprophytic bark beetles that utilize kairomones (host volatiles). We present the results of a mark-recapture experiment that examined adult dispersal patterns of the saprophytic bark beetle Hylurgus ligniperda. Releases took place in summer and autumn 2014, in a clearcut pine forest in the central North Island, New Zealand. Both flight-experienced and flight-naïve adults were marked and released in the center of a circular trap grid that extended to 960 m with 170 or 200 panel traps baited with a kairomone blend of alpha-pinene and ethanol. Of the 18,464 released H. ligniperda, 9,209 (49.9%) of the beetles flew, and 96 (1.04%) of the beetles that flew were recaptured. Individuals were recaptured at all distances. The recapture of flight-experienced beetles declined with dispersal distance, and a diffusion model showed heterogeneous dispersal tendencies within the population. Our best model estimated that 46% of flight-experienced beetles disperse > 1 km, and 1.6% > 5 km. Conversely, no declining pattern was shown in the recapture of flight-naïve beetles, suggesting that emerging H. ligniperda may require a period of flight to initiate chemotropic orientation behavior and subsequent attraction to traps. We discuss the implications of these findings for the management of phytosanitary risks. For instance, combining landscape knowledge of source populations with dispersal processes facilitates estimation of pest pressure at economically sensitive areas such as harvest and timber storage sites. Quantitative dispersal estimates also inform pest risk assessments by predicting spread rates for H. ligniperda that has proven establishment capabilities in other countries.

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

Publications

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

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