Dataset Information

Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest.

ABSTRACT: The phyllosphere--the aerial surfaces of plants, including leaves--is a ubiquitous global habitat that harbors diverse bacterial communities. Phyllosphere bacterial communities have the potential to influence plant biogeography and ecosystem function through their influence on the fitness and function of their hosts, but the host attributes that drive community assembly in the phyllosphere are poorly understood. In this study we used high-throughput sequencing to quantify bacterial community structure on the leaves of 57 tree species in a neotropical forest in Panama. We tested for relationships between bacterial communities on tree leaves and the functional traits, taxonomy, and phylogeny of their plant hosts. Bacterial communities on tropical tree leaves were diverse; leaves from individual trees were host to more than 400 bacterial taxa. Bacterial communities in the phyllosphere were dominated by a core microbiome of taxa including Actinobacteria, Alpha-, Beta-, and Gammaproteobacteria, and Sphingobacteria. Host attributes including plant taxonomic identity, phylogeny, growth and mortality rates, wood density, leaf mass per area, and leaf nitrogen and phosphorous concentrations were correlated with bacterial community structure on leaves. The relative abundances of several bacterial taxa were correlated with suites of host plant traits related to major axes of plant trait variation, including the leaf economics spectrum and the wood density-growth/mortality tradeoff. These correlations between phyllosphere bacterial diversity and host growth, mortality, and function suggest that incorporating information on plant-microbe associations will improve our ability to understand plant functional biogeography and the drivers of variation in plant and ecosystem function.

SUBMITTER: Kembel SW

PROVIDER: S-EPMC4183302 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest.

Kembel Steven W SW O'Connor Timothy K TK Arnold Holly K HK Hubbell Stephen P SP Wright S Joseph SJ Green Jessica L JL

Proceedings of the National Academy of Sciences of the United States of America 20140915 38

The phyllosphere--the aerial surfaces of plants, including leaves--is a ubiquitous global habitat that harbors diverse bacterial communities. Phyllosphere bacterial communities have the potential to influence plant biogeography and ecosystem function through their influence on the fitness and function of their hosts, but the host attributes that drive community assembly in the phyllosphere are poorly understood. In this study we used high-throughput sequencing to quantify bacterial community str ...[more]

PMID: 25225376

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Project description:BackgroundPhyllosphere microbes play important roles in host plant performance and fitness. Recent studies have suggested that tropical and temperate forests harbor diverse phyllosphere bacterial and fungal communities and their assembly is driven by host species identity and plant traits. However, no study has yet examined how seasonality (e.g. dry vs. wet seasons) influences phyllosphere microbial community assembly in natural forests. In addition, in subtropical forests characterized as the transitional zonal vegetation type from tropical to temperate forests, how tree phyllosphere microbial communities are assembled remains unknown. In this study, we quantified bacterial and fungal community structure and diversity on the leaves of 45 tree species with varying phylogenetic identities and importance values within a 20-ha lower subtropical evergreen broad-leaved forest plot in dry and wet seasons. We explored if and how the microbial community assembly varies with host species identity, plant traits and seasonality.ResultsPhyllosphere microbial communities in the subtropical forest are more abundant and diverse than those in tropical and temperate forests, and the tree species share a "core microbiome" in either bacteria or fungi. Variations in phyllosphere bacterial and fungal community assembly are explained more by host species identity than by seasonality. There is a strong clustering of the phyllosphere microbial assemblage amongst trees by seasonality, and the seasonality effects are more pronounced on bacterial than fungal community assembly. Host traits have different effects on community compositions and diversities of both bacteria and fungi, and among them calcium concentration and importance value are the most powerful explaining variables for bacteria and fungi, respectively. There are significant evolutionary associations between host species and phyllosphere microbiome.ConclusionsOur results suggest that subtropical tree phyllosphere microbial communities vary with host species identity, plant traits and seasonality. Host species identity, compared to seasonality, has greater effects on phyllosphere microbial community assembly, and such effects differ between bacterial and fungal communities. These findings advance our understanding of the patterns and drivers of phyllosphere microbial community assembly in zonal forests at a global scale.

Project description:BACKGROUND:The phyllosphere is an important microbial habitat, but our understanding of how plant hosts drive the composition of their associated leaf microbial communities and whether taxonomic associations between plants and phyllosphere microbes represent adaptive matching remains limited. In this study, we quantify bacterial functional diversity in the phyllosphere of 17 tree species in a diverse neotropical forest using metagenomic shotgun sequencing. We ask how hosts drive the functional composition of phyllosphere communities and their turnover across tree species, using host functional traits and phylogeny. RESULTS:Neotropical tree phyllosphere communities are dominated by functions related to the metabolism of carbohydrates, amino acids, and energy acquisition, along with environmental signalling pathways involved in membrane transport. While most functional variation was observed within communities, there is non-random assembly of microbial functions across host species possessing different leaf traits. Metabolic functions related to biosynthesis and degradation of secondary compounds, along with signal transduction and cell-cell adhesion, were particularly important in driving the match between microbial functions and host traits. These microbial functions were also evolutionarily conserved across the host phylogeny. CONCLUSIONS:Functional profiling based on metagenomic shotgun sequencing offers evidence for the presence of a core functional microbiota across phyllosphere communities of neotropical trees. While functional turnover across phyllosphere communities is relatively small, the association between microbial functions and leaf trait gradients among host species supports a significant role for plant hosts as selective filters on phyllosphere community assembly. This interpretation is supported by the presence of phylogenetic signal for the microbial traits driving inter-community variation across the host phylogeny. Taken together, our results suggest that there is adaptive matching between phyllosphere microbes and their plant hosts. Video abstract.

Project description:Phyllosphere microbial communities are increasingly experiencing intense pulse disturbance events such as drought. It is currently unknown how phyllosphere communities respond to such disturbances and if they are able to recover. We explored the stability of phyllosphere communities over time, in response to drought stress, and under recovery from drought on temperate forage grasses. Compositional or functional changes were observed during the disturbance period and whether communities returned to non-stressed levels following recovery. Here, we found that phyllosphere community composition shifts as a result of simulated drought but does not fully recover after irrigation is resumed and that the degree of community response to drought is host species dependent. However, while community composition had changed, we found a high level of functional stability (resistance) over time and in the water deficit treatment. Ecological modeling enabled us to understand community assembly processes over a growing season and to determine if they were disrupted during a disturbance event. Phyllosphere community succession was characterized by a strong level of ecological drift, but drought disturbance resulted in variable selection, or, in other words, communities were diverging due to differences in selective pressures. This successional divergence of communities with drought was unique for each host species. Understanding phyllosphere responses to environmental stresses is important as climate change-induced stresses are expected to reduce crop productivity and phyllosphere functioning.ImportanceLeaf surface microbiomes have the potential to influence agricultural and ecosystem productivity. We assessed their stability by determining composition, functional resistance, and resilience. Resistance is the degree to which communities remain unchanged as a result of disturbance, and resilience is the ability of a community to recover to pre-disturbance conditions. By understanding the mechanisms of community assembly and how they relate to the resistance and resilience of microbial communities under common environmental stresses such as drought, we can better understand how communities will adapt to a changing environment and how we can promote healthy agricultural microbiomes. In this study, phyllosphere compositional stability was highly related to plant host species phylogeny and, to a lesser extent, known stress tolerances. Phyllosphere community assembly and stability are a result of complex interactions of ecological processes that are differentially imposed by host species.

Project description:In the context of secondary forest succession, aboveground-belowground interactions are known to affect the dynamics and functional structure of plant communities. However, the links between soil microbial communities, soil abiotic properties, plant functional traits in the case of semi-arid and arid ecosystems, are unclear. In this study, we investigated the changes in soil microbial species diversity and community composition, and the corresponding effects of soil abiotic properties and plant functional traits, during a ≥150-year secondary forest succession on the Loess Plateau, which represents a typical semi-arid ecosystem in China. Plant community fragments were assigned to six successional stages: 1-4, 4-8, 8-15, 15-50, 50-100, and 100-150 years after abandonment. Bacterial and fungal communities were analyzed by high-throughput sequencing of the V4 hypervariable region of the 16S rRNA gene and the internal transcribed spacer (ITS2) region of the rRNA operon, respectively. A multivariate variation-partitioning approach was used to estimate the contributions of soil properties and plant traits to the observed microbial community composition. We found considerable differences in bacterial and fungal community compositions between the early (S1-S3) and later (S4-S6) successional stages. In total, 18 and 12 unique families were, respectively, obtained for bacteria and fungi, as indicators of microbial community succession across the six stages. Bacterial alpha diversity was positively correlated with plant species alpha diversity, while fungal diversity was negatively correlated with plant species diversity. Certain fungal and bacterial taxa appeared to be associated with the occurrence of dominant plant species at different successional stages. Soil properties (pH, total N, total C, NH4-N, NO3-N, and PO4-P concentrations) and plant traits explained 63.80% and 56.68% of total variance in bacterial and fungal community compositions, respectively. These results indicate that soil microbial communities are coupled with plant communities via the mediation of microbial species diversity and community composition over a long-term secondary forest succession in the semi-arid ecosystem. The bacterial and fungal communities show distinct patterns in response to plant community succession, according to both soil abiotic properties and plant functional traits.

Project description:The use of plant traits to predict ecosystem functions has been gaining growing attention. Above-ground plant traits, such as leaf nitrogen (N) content and specific leaf area (SLA), have been shown to strongly relate to ecosystem productivity, respiration and nutrient cycling. Furthermore, increasing plant functional trait diversity has been suggested as a possible mechanism to increase ecosystem carbon (C) storage. However, it is uncertain whether below-ground plant traits can be predicted by above-ground traits, and if both above- and below-ground traits can be used to predict soil properties and ecosystem-level functions.Here, we used two adjacent field experiments in temperate grassland to investigate if above- and below-ground plant traits are related, and whether relationships between plant traits, soil properties and ecosystem C fluxes (i.e. ecosystem respiration and net ecosystem exchange) measured in potted monocultures could be detected in mixed field communities.We found that certain shoot traits (e.g. shoot N and C, and leaf dry matter content) were related to root traits (e.g. root N, root C:N and root dry matter content) in monocultures, but such relationships were either weak or not detected in mixed communities. Some relationships between plant traits (i.e. shoot N, root N and/or shoot C:N) and soil properties (i.e. inorganic N availability and microbial community structure) were similar in monocultures and mixed communities, but they were more strongly linked to shoot traits in monocultures and root traits in mixed communities. Structural equation modelling showed that above- and below-ground traits and soil properties improved predictions of ecosystem C fluxes in monocultures, but not in mixed communities on the basis of community-weighted mean traits. Synthesis. Our results from a single grassland habitat detected relationships in monocultures between above- and below-ground plant traits, and between plant traits, soil properties and ecosystem C fluxes. However, these relationships were generally weaker or different in mixed communities. Our results demonstrate that while plant traits can be used to predict certain soil properties and ecosystem functions in monocultures, they are less effective for predicting how changes in plant species composition influence ecosystem functions in mixed communities.

Project description:BackgroundThe different hypotheses proposed to explain positive species richness-productivity relationships, i.e. selection effect and complementarity effect, imply that plant functional characteristics are at the core of a mechanistic understanding of biodiversity effects.Methodology/principal findingsWe used two community-wide measures of plant functional composition, (1) community-weighted means of trait values (CWM) and (2) functional trait diversity based on Rao's quadratic diversity (FD(Q)) to predict biomass production and measures of biodiversity effects in experimental grasslands (Jena Experiment) with different species richness (2, 4, 8, 16 and 60) and different functional group number and composition (1 to 4; legumes, grasses, small herbs, tall herbs) four years after establishment. Functional trait composition had a larger predictive power for community biomass and measures of biodiversitity effects (40-82% of explained variation) than species richness per se (<1-13% of explained variation). CWM explained a larger amount of variation in community biomass (80%) and net biodiversity effects (70%) than FD(Q) (36 and 38% of explained variation respectively). FD(Q) explained similar proportions of variation in complementarity effects (24%, positive relationship) and selection effects (28%, negative relationship) as CWM (27% of explained variation for both complementarity and selection effects), but for all response variables the combination of CWM and FD(Q) led to significant model improvement compared to a separate consideration of different components of functional trait composition. Effects of FD(Q) were mainly attributable to diversity in nutrient acquisition and life-history strategies. The large spectrum of traits contributing to positive effects of CWM on biomass production and net biodiversity effects indicated that effects of dominant species were associated with different trait combinations.Conclusions/significanceOur results suggest that the identification of relevant traits and the relative impacts of functional identity of dominant species and functional diversity are essential for a mechanistic understanding of the role of plant diversity for ecosystem processes such as aboveground biomass production.

Project description:BackgroundThe phyllosphere microbiome is crucial for plant health and ecosystem functioning. While host species play a determining role in shaping the phyllosphere microbiome, host trees of the same species that are subjected to different environmental conditions can still exhibit large degrees of variation in their microbiome diversity and composition. Whether these intra-specific variations in phyllosphere microbiome diversity and composition can be observed over the broader expanse of forest landscapes remains unclear. In this study, we aim to assess the variation in the top canopy phyllosphere bacterial communities between and within host tree species in the temperate European forests, focusing on Fagus sylvatica (European beech) and Picea abies (Norway spruce).ResultsWe profiled the bacterial diversity, composition, driving factors, and discriminant taxa in the top canopy phyllosphere of 211 trees in two temperate forests, Veluwe National Parks, the Netherlands and Bavarian Forest National Park, Germany. We found the bacterial communities were primarily shaped by host species, and large variation existed within beech and spruce. While we showed that there was a core microbiome in all tree species examined, community composition varied with elevation, tree diameter at breast height, and leaf-specific traits (e.g., chlorophyll and P content). These driving factors of bacterial community composition also correlated with the relative abundance of specific bacterial families.ConclusionsWhile our results underscored the importance of host species, we demonstrated a substantial range of variation in phyllosphere bacterial diversity and composition within a host species. Drivers of these variations have implications at both the individual host tree level, where the bacterial communities differed based on tree traits, and at the broader forest landscape level, where drivers like certain highly plastic leaf traits can potentially link forest canopy bacterial community variations to forest ecosystem processes. We eventually showed close associations between forest canopy phyllosphere bacterial communities and host trees exist, and the consistent patterns emerging from these associations are critical for host plant functioning.

Dataset Information

Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest.

Publications

Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest.

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