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Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions.

ABSTRACT: Traits that permit successful invasions have often seemed idiosyncratic, and the key biological traits identified vary widely among species. This fundamentally limits our ability to determine the invasion potential of a species. However, ultimately, successful invaders must have positive growth rates that longer term result in higher biomass accumulation than competing established species. In many terrestrial ecosystems nitrogen limits plant growth, and is a key factor determining productivity and the outcome of competition among species. Plant nitrogen use may provide a powerful framework to evaluate the invasive potential of a species in nitrogen-limiting ecosystems. Six mechanisms influence plant nitrogen use or acquisition: photosynthetic tissue allocation, photosynthetic nitrogen use efficiency, nitrogen fixation, nitrogen-leaching losses, gross nitrogen mineralization, and plant nitrogen residence time. Here we show that among these alternatives, the key mechanism allowing invasion for Pinus strobus into nitrogen limited grasslands was its higher nitrogen residence time. This higher nitrogen residence time created a positive feedback that redistributed nitrogen from the soil into the plant. This positive feedback allowed P. strobus to accumulate twice as much nitrogen in its tissues and four times as much nitrogen to photosynthetic tissues, as compared with other plant species. In turn, this larger leaf nitrogen pool increased total plant carbon gain of P. strobus two- to sevenfold as compared with other plant species. Thus our data illustrate that plant species can change internal ecosystem nitrogen cycling feedbacks and this mechanism can allow them to gain a competitive advantage over other plant species.

SUBMITTER: Laungani R

PROVIDER: S-EPMC2718360 | biostudies-literature | 2009 Jul

REPOSITORIES: biostudies-literature

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Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions.

Laungani Ramesh R Knops Johannes M H JM

Proceedings of the National Academy of Sciences of the United States of America 20090710 30

Traits that permit successful invasions have often seemed idiosyncratic, and the key biological traits identified vary widely among species. This fundamentally limits our ability to determine the invasion potential of a species. However, ultimately, successful invaders must have positive growth rates that longer term result in higher biomass accumulation than competing established species. In many terrestrial ecosystems nitrogen limits plant growth, and is a key factor determining productivity a ...[more]

PMID: 19592506

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Project description:In monoculture, certain plant species are able to preferentially utilize different nitrogen (N) forms, both inorganic and organic, including amino acids and peptides, thus forming fundamental niches based on the chemical form of N. Results from field studies, however, are inconsistent: Some showing that coexisting plant species predominantly utilize inorganic N, while others reveal distinct interspecies preferences for different N forms. As a result, the extent to which hypothetical niches are realized in nature remains unclear. Here, we used in situ stable isotope tracer techniques to test the idea, in temperate grassland, that niche partitioning of N based on chemical form is related to plant productivity and the relative availability of organic and inorganic N. We also tested in situ whether grassland plants vary in their ability to compete for, and utilize peptides, which have recently been shown to act as an N source for plants in strongly N-limited ecosystems. We hypothesized that plants would preferentially use NO3 (-)-N and NH4 (+)-N over dissolved organic N in high-productivity grassland where inorganic N availability is high. On the other hand, in low-productivity grasslands, where the availability of dissolved inorganic N is low, and soil availability of dissolved organic N is greater, we predicted that plants would preferentially use N from amino acids and peptides, prior to microbial mineralization. Turves from two well-characterized grasslands of contrasting productivity and soil N availability were injected, in situ, with mixtures of (15)N-labeled inorganic N (NO3 (-) and NH4 (+)) and (13)C(15)N labeled amino acid (l-alanine) and peptide (l-tri-alanine). In order to measure rapid assimilation of these N forms by soil microbes and plants, the uptake of these substrates was traced within 2.5 hours into the shoots of the most abundant plant species, as well as roots and the soil microbial biomass. We found that, contrary to our hypothesis, the majority of plant species across both grasslands took up most N in the form of NH4 (+), suggesting that inorganic N is their predominant N source. However, we did find that organic N was a source of N which could be utilized by plant species at both sites, and in the low-productivity grassland, plants were able to capture some tri-alanine-N directly. Although our findings did not support the hypothesis that differences in the availability of inorganic and organic N facilitate resource partitioning in grassland, they do support the emerging view that peptides represent a significant, but until now neglected, component of the terrestrial N cycle.

Project description:BACKGROUND:Rhizosphere microbial communities are key regulators of plant performance, yet few studies have assessed the impact of different management approaches on the rhizosphere microbiomes of major crops. Rhizosphere microbial communities are shaped by interactions between agricultural management and host selection processes, but studies often consider these factors individually rather than in combination. We tested the impacts of management (M) and rhizosphere effects (R) on microbial community structure and co-occurrence networks of maize roots collected from long-term conventionally and organically managed maize-tomato agroecosystems. We also explored the interaction between these factors (M × R) and how it impacts rhizosphere microbial diversity and composition, differential abundance, indicator taxa, co-occurrence network structure, and microbial nitrogen-cycling processes. RESULTS:Host selection processes moderate the influence of agricultural management on rhizosphere microbial communities, although bacteria and fungi respond differently to plant selection and agricultural management. We found that plants recruit management-system-specific taxa and shift N-cycling pathways in the rhizosphere, distinguishing this soil compartment from bulk soil. Rhizosphere microbiomes from conventional and organic systems were more similar in diversity and network structure than communities from their respective bulk soils, and community composition was affected by both M and R effects. In contrast, fungal community composition was affected only by management, and network structure only by plant selection. Quantification of six nitrogen-cycling genes (nifH, amoA [bacterial and archaeal], nirK, nrfA, and nosZ) revealed that only nosZ abundance was affected by management and was higher in the organic system. CONCLUSIONS:Plant selection interacts with conventional and organic management practices to shape rhizosphere microbial community composition, co-occurrence patterns, and at least one nitrogen-cycling process. Reframing research priorities to better understand adaptive plant-microbe feedbacks and include roots as a significant moderating influence of management outcomes could help guide plant-oriented strategies to improve productivity and agroecosystem sustainability.

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Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions.

Publications

Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions.

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