An official website of the United States government
Summary Habitat fragmentation is a leading cause of biodiversity and ecosystem function loss in the Anthropocene. Despite the importance of plant–microbiome interactions to ecosystem productivity, we have limited knowledge of how fragmentation affects microbiomes and even less knowledge of its consequences for microbial interactions with plants.Combining field surveys, microbiome sequencing, manipulative experiments, and random forest models, we investigated fragmentation legacy effects on soil microbiomes in imperiled pine rocklands, tested how compositional shifts across 14 fragmentation‐altered soil microbiomes affected performance and resource allocation of three native plant species, and identified fragmentation‐responding microbial families underpinning plant performance.Legacies of habitat fragmentation were associated with significant changes in microbial diversity and composition (across three of four community axes). Experiments showed plants often strongly benefited from the microbiome’s presence, but fragmentation‐associated changes in microbiome composition also significantly affected plant performance and resource allocation across all seven metrics examined. Finally, random forest models identified ten fungal and six bacterial families important for plant performance that changed significantly with fragmentation.Our findings not only support the existence of significant fragmentation effects on natural microbiomes, but also demonstrate for the first time that fragmentation‐associated changes in microbiomes can have meaningful consequences for native plant performance and investment.
more »
« less
Hydrology shapes microbial communities and microbiome‐mediated growth of an Everglades tree island species
Plant‐associated microbiomes can improve plant fitness by ameliorating environmental stress, providing a promising avenue for improving outplantings during restoration. However, the effects of water management on these microbial communities and their cascading effects on primary producers are unresolved for many imperiled ecosystems. One such habitat, Everglades tree islands, has declined by 54% in some areas, releasing excess nutrients into surrounding wetlands and exacerbating nutrient pollution. We conducted a factorial experiment, manipulating the soil microbiome and hydrological regime experienced by a tree island native,Ficus aurea, to determine how microbiomes impact growth under two hydrological management plans. All plants were watered to simulate natural precipitation, but plants in the “unconstrained” management treatment were allowed to accumulate water above the soil surface, while the “constrained” treatment had a reduced stage to avoid soil submersion. We found significant effects of the microbiomes on overall plant performance and aboveground versus belowground investment; however, these effects depended on hydrological treatment. For instance, microbiomes increased investment in roots relative to aboveground tissues, but these effects were 142% stronger in the constrained compared to unconstrained water regime. Changes in hydrology also resulted in changes in the prokaryotic community composition, including a >20 log2fold increase in the relative abundance of Rhizobiaceae, and hydrology‐shifted microbial composition was linked to changes in plant performance. Our results suggest that differences in hydrological management can have important effects on microbial communities, including taxa often involved in nitrogen cycling, which can in turn impact plant performance.
more »
« less
- PAR ID:
- 10392594
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Restoration Ecology
- Volume:
- 31
- Issue:
- 1
- ISSN:
- 1061-2971
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract As ecosystems face unprecedented change and habitat loss, pursuing comprehensive and resilient habitat restoration will be integral to protecting and maintaining natural areas and the services they provide. Microbiomes offer an important avenue for improving restoration efforts as they are integral to ecosystem health and functioning. Despite microbiomes' importance, unresolved knowledge gaps hinder their inclusion in restoration efforts. Here, we address two critical gaps in understanding microbial roles in restoration—fungal microbiomes' importance in “reconstructive” restoration efforts and how management and restoration decisions interactively impact fungal communities and their cascading effects on trees. We combined field surveys, microbiome sequencing, and greenhouse experiments to determine how reconstructing an iconic landscape feature—tree islands—in the highly imperiled Everglades impacts fungal microbiomes and fungal effects on native tree species compared with their natural counterparts under different proposed hydrological management regimes. Constructed islands used in this research were built from peat soil and limestone collected from deep sloughs and levees nearby the restoration sites in 2003, providing 18 years for microbiome assembly on constructed islands. We found that while fungal microbiomes from natural and constructed tree islands exhibited similar diversity and richness, they differed significantly in community composition. These compositional differences arose mainly from changes to which fungal taxa were present on the islands rather than changes in relative abundances. Surprisingly, ~50% of fungal hub taxa (putative keystone fungi) from natural islands were missing on constructed islands, suggesting that differences in community composition of constructed island could be important for microbiome stability and function. The differences in fungal composition between natural and constructed islands had important consequences for tree growth. Specifically, these compositional differences interacted with hydrological regime (treatments simulating management strategies) to affect woody growth across the four tree species in our experiment. Taken together, our results demonstrate that reconstructing a landscape feature without consideration of microbiomes can result in diverging fungal communities that are likely to interact with management decisions leading to meaningful consequences for foundational primary producers. Our results recommend cooperation between restoration practitioners and ecologists to evaluate opportunities for active management and restoration of microbiomes during future reconstructive restoration.more » « less
-
Abstract Decadal scale lake drying in interior Alaska results in lake margin colonization by willow shrub and graminoid vegetation, but the effects of these changes on plant production, biodiversity, soil properties, and soil microbial communities are not well known. We studied changes in soil organic carbon (SOC) and nitrogen (N) storage, plant and microbial community composition, and soil microbial activities in drying and non‐drying lakes in the Yukon Flats National Wildlife Refuge. Historic changes in lake area were determined using Landsat imagery. Results showed that SOC storage in drying lake margins declined by 0.13 kg C m−2 yr−1over 30 years of exposure of lake sediments, with no significant change in soil N. Lake drying resulted in an increase in graminoid and shrub aboveground net primary production (ANPP, +3% yr−1) with little change in plant functional composition. Increases in ANPP were similar in magnitude (but opposite in sign) to losses in SOC over a 30‐year drying trend. Potential decomposition rates and soil enzyme activities were lower in drying lake margins compared to stable lake margins, possibly due to high salinities in drying lake margin soils. Microbial communities shifted in response to changing plant communities, although they still retained a legacy of the previous plant community. Understanding how changing lake hydrology impacts the ecology and biogeochemistry of lake margin terrestrial ecosystems is an underexamined phenomenon with large impacts to landscape processes.more » « less
-
Abstract Efforts to catalog global biodiversity have often focused on aboveground taxonomic diversity, with limited consideration of belowground communities. However, diversity aboveground may influence the diversity of belowground communities and vice versa. In addition to taxonomic diversity, the structural diversity of plant communities may be related to the diversity of soil bacterial and fungal communities, which drive important ecosystem processes but are difficult to characterize across broad spatial scales. In forests, canopy structural diversity may influence soil microorganisms through its effects on ecosystem productivity and root architecture, and via associations between canopy structure, stand age, and species richness. Given that structural diversity is one of the few types of diversity that can be readily measured remotely (e.g., using light detection and ranging—LiDAR), establishing links between structural and microbial diversity could facilitate the detection of belowground biodiversity hotspots. We investigated the potential for using remotely sensed information about forest structural diversity as a predictor of soil microbial community richness and composition. We calculated LiDAR‐derived metrics of structural diversity as well as a suite of stand and soil properties from 38 forested plots across the central hardwoods region of Indiana, USA, to test whether forest canopy structure is linked with the community richness and diversity of four key soil microbial groups: bacteria, fungi, arbuscular mycorrhizal (AM) fungi, and ectomycorrhizal (EM) fungi. We found that the density of canopy vegetation is positively associated with the taxonomic richness (alpha diversity) of EM fungi, independent of changes in plant taxonomic richness. Further, structural diversity metrics were significantly correlated with the overall community composition of bacteria, EM, and total fungal communities. However, soil properties were the strongest predictors of variation in the taxonomic richness and community composition of microbial communities in comparison with structural diversity and tree species diversity. As remote sensing tools and algorithms are rapidly advancing, these results may have important implications for the use of remote sensing of vegetation structural diversity for management and restoration practices aimed at preserving belowground biodiversity.more » « less
-
Coastal wetlands can store carbon by sequestering more carbon through primary production than they release though biogenic greenhouse gas production. The joint effects of saltwater intrusion and sea level rise (SWISLR) and changing precipitation patterns alter sulfate and oxygen availability, challenging estimates of biogenic greenhouse gas emissions. Iron-rich soils have been shown to buffer soil sulfidization by sequestering sulfide into iron-sulfide. But as SWISLR increases soil sulfate concentrations, sulfide produced via sulfate reduction will likely exceed the buffering capacity of soil iron, allowing toxic sulfide levels to accumulate. We used a soil mesocosm approach to examine the influence of hydrology (wet, dry, interim) and plant presence (with or without plants) on wetland soils sourced from different hydrologic histories at a restored coastal wetland. We hypothesized that reducing conditions (i.e., flooded, no plants) impact anaerobic metabolisms similarly, whereas oxidizing conditions (i.e., dry, plant presence) disrupt coupled sulfate reduction and iron reduction. Over eight weeks of hydrologic manipulation, 16S rRNA amplicon sequencing and shotgun metagenomic sequencing were used to characterize microbial communities, while greenhouse gas fluxes, soil redox potential, and physicochemical properties were measured. Results showed that contemporary hydrologic treatment affected assimilatory sulfate reduction gene composition, and hydrologic history influenced dissimilatory sulfate reduction and iron reduction gene composition. Sulfate and iron reduction genes were correlated, and dissimilatory sulfate reduction genes explained variance in methane fluxes. These findings highlight the role of historical hydrology, potential saltwater exposure, and soil iron in shaping microbial responses to future changes in soil moisture and salinity.more » « less
