Publications

2021

Microbiome-mediated response to pulse fire disturbance outweighs the effects of fire legacy on plant performance

New Phytologist, 2021, https://doi.org/10.1111/nph.17689

Abstract

  • Fire plays a major role in structuring plant communities across the globe. Interactions with soil microbes impact plant fitness, scaling up to influence plant populations and distributions. Here we present the first factorial manipulation of both fire and soil microbiome presence to investigate their interactive effects on plant performance across a suite of plant species with varying life history traits.
  • We conducted fully-factorial experiments on each of 11 species from the Florida scrub ecosystem to test plant performance responses to soils with varying fire histories (36 soil sources), the presence/absence of a microbiome, and exposure to an experimental burn.
  • Results revealed interactive ‘pulse’ effects between fire and the soil microbiome on plant performance. On average, post-fire soil microbiomes strongly reduced plant productivity compared to unburned or sterilized soils. Interestingly, longer-term fire ‘legacy’ effects had minor impacts on plant performance and were unrelated to soil microbiomes.
  • While pulse fire effects on plant-microbiome interactions are short-term, they could have long-term consequences for plant communities by establishing differential microbiome-mediated priority effects during post-disturbance succession. The prominence of pulse fire effects on plant-microbe interactions has even greater import due to expected increases in fire disturbances resulting from anthropogenic climate change.

2020

Tripartite mutualisms as models for understanding plant–microbial interactions

Current Opinion in Plant Biology, 2020, 10.1016/j.pbi.2020.02.003

Abstract

All plants host diverse microbial assemblages that shape plant health, productivity, and function. While some microbial effects are attributable to particular symbionts, interactions among plant-associated microbes can nonadditively affect plant fitness and traits in ways that cannot be predicted from pairwise interactions. Recent research into tripartite plant–microbe mutualisms has provided crucial insight into this nonadditivity and the mechanisms underlying plant interactions with multiple microbes. Here, we discuss how interactions among microbial mutualists affect plant performance, highlight consequences of biotic and abiotic context-dependency for nonadditive outcomes, and summarize burgeoning efforts to determine the molecular bases of how plants regulate establishment, resource exchange, and maintenance of tripartite interactions. We conclude with four goals for future tripartite studies that will advance our overall understanding of complex plant–microbial interactions.

2019

Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks

Frontiers in Plant Science, 2019, 10.3389/fpls.2019.01018

Abstract

Plants may actively cultivate microorganisms in their roots and rhizosphere that enhance their nutrition. To develop cropping strategies that substitute mineral fertilizers for beneficial root symbioses, we must first understand how microbial communities associated with plant roots differ among plant taxa and how they respond to fertilization. Arbuscular mycorrhizal (AM) fungi and rhizobacteria are of particular interest because they enhance nutrient availability to plants and perform a suite of nutrient cycling functions. The purpose of this experiment is to examine the root and soil microbiome in a long- term switchgrass (Panicum virgatum) biofuel feedstock experiment and determine how AM fungi and rhizobacteria respond to plant diversity and soil fertility. We hypothesize that intra- and interspecific plant diversity, nitrogen fertilization (+N), and their interaction will influence the biomass and community composition of AM fungi and rhizobacteria. We further hypothesize that +N will reduce the abundance of nitrogenase-encoding nifH genes on the rhizoplane. Roots and soils were sampled from three switchgrass cultivars (Cave-in-Rock, Kanlow, Southlow) grown in monoculture, intraspecific mixture, and interspecific planting mixtures with either Andropogon gerardii or diverse native tallgrass prairie species. Molecular sequencing was performed on root and soil samples, fatty acid extractions were assessed to determine microbial biomass, and quantitative polymerase chain reaction (qPCR) was performed on nifH genes from the rhizoplane. Sequence data determined core AM fungal and bacterial microbiomes and indicator taxa for plant diversity and +N treatments. We found that plant diversity and +N influenced AM fungal biomass and community structure. Across all plant diversity treatments, +N reduced the biomass of AM fungi and nifH gene abundance by more than 40%. The AM fungal genus Scutellospora was an indicator for +N, with relative abundance significantly greater under +N and in monoculture treatments. Community composition of rhizobacteria was influenced by plant diversity but not by +N. Verrucomicrobia and Proteobacteria were the dominant bacterial phyla in both roots and soils. Our findings provide evidence that soil fertility and plant diversity structure the root and soil microbiome. Optimization of soil communities for switchgrass production must take into account differences among cultivars and their unique responses to shifts in soil fertility.

2018

Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest

The ISME Journal , 2018, doi: 10.1038/s41396-018-0189-7

Abstract

Improved understanding of the nutritional ecology of arbuscular mycorrhizal (AM) fungi is important in understanding how tropical forests maintain high productivity on low-fertility soils. Relatively little is known about how AM fungi will respond to changes in nutrient inputs in tropical forests, which hampers our ability to assess how forest productivity will be influenced by anthropogenic change. Here we assessed the influence of long-term inorganic and organic nutrient additions and nutrient depletion on AM fungi, using two adjacent experiments in a lowland tropical forest in Panama. We characterised AM fungal communities in soil and roots using 454-pyrosequencing, and quantified AM fungal abundance using microscopy and a lipid biomarker. Phosphorus and nitrogen addition reduced the abundance of AM fungi to a similar extent, but affected community composition in different ways. Nutrient depletion (removal of leaf litter) had a pronounced effect on AM fungal community composition, affecting nearly as many OTUs as phosphorus addition. The addition of nutrients in organic form (leaf litter) had little effect on any AM fungal parameter. Soil AM fungal communities responded more strongly to changes in nutrient availability than communities in roots. This suggests that the ‘dual niches’ of AM fungi in soil versus roots are structured to different degrees by abiotic environmental filters, and biotic filters imposed by the plant host. Our findings indicate that AM fungal communities are fine-tuned to nutrient regimes, and support future studies aiming to link AM fungal community dynamics with ecosystem function.

2017

A phosphorus threshold for mycoheterotrophic plants in tropical forests

Proceedings of the Royal Society B, 2017, doi: 10.1098/rspb.2016.2093

Abstract

The majority of terrestrial plants associate with arbuscular mycorrhizal (AM) fungi, which typically facilitate the uptake of limiting mineral nutrients by plants in exchange for plant carbon. However, hundreds of non-photosynthetic plant species—mycoheterotrophs—depend entirely on AM fungi for carbon as well as mineral nutrition. Mycoheterotrophs can provide insight into the operation and regulation of AM fungal relationships, but little is known about the factors, fungal or otherwise, that affect mycoheterotroph abundance and distribution. In a lowland tropical forest in Panama, we conducted the first systematic investigation into the influence of abiotic factors on the abundance and distribution of mycoheterotrophs, to ask whether the availability of nitrogen and phosphorus altered the occurrence of mycoheterotrophs and their AM fungal partners. Across a natural fertility gradient spanning the isthmus of Panama, and also in a long-term nutrient-addition experiment, mycoheterotrophs were entirely absent when soil exchangeable phosphate concentrations exceeded 2 mg P kg−1. Experimental phosphorus addition reduced the abundance of AM fungi, and also reduced the abundance of the specific AM fungal taxa required by the mycoheterotrophs, suggesting that the phosphorus sensitivity of mycoheterotrophs is underpinned by the phosphorus sensitivity of their AM fungal hosts. The soil phosphorus concentration of 2 mg P kg−1 also corresponds to a marked shift in tree community composition and soil phosphatase activity across the fertility gradient, suggesting that our findings have broad ecological significance.

Arbuscular mycorrhizal fungal community composition is altered by long-term litter removal but not litter addition in a lowland tropical forest

New Phytologist, 2017, doi: 10.1111/nph.14384

Summary

  • Tropical forest productivity is sustained by the cycling of nutrients through decomposing organic matter. Arbuscular mycorrhizal (AM) fungi play a key role in the nutrition of tropical trees, yet there has been little experimental investigation into the role of AM fungi in nutrient cycling via decomposing organic material in tropical forests.
  • We evaluated the responses of AM fungi in a long-term leaf litter addition and removal experiment in a tropical forest in Panama. We described AM fungal communities using 454-pyrosequencing, quantified the proportion of root length colonised by AM fungi using microscopy, and estimated AM fungal biomass using a lipid biomarker.
  • AM fungal community composition was altered by litter removal but not litter addition. Root colonisation was substantially greater in the superficial organic layer compared with the mineral soil. Overall colonisation was lower in the litter removal treatment, which lacked an organic layer. There was no effect of litter manipulation on the concentration of the AM fungal lipid biomarker in the mineral soil.
  • We hypothesise that reductions in organic matter brought about by litter removal may lead to AM fungi obtaining nutrients from recalcitrant organic or mineral sources in the soil, besides increasing fungal competition for progressively limited resources.

2016

Plant-Soil Feedback Special Feature

The role of locally adapted mycorrhizas and rhizobacteria in plant-soil feedback systems 

Functional Ecology, 2016, 30: 1086-1098

Abstract

  1. The plant–soil feedback (PSF) framework has become an important theory in plant ecology, yet many ecological and evolutionary factors that influence PSFs have yet to be fully considered. Here, we discuss the importance of local adaptation among plants and root-associated fungi and bacteria. Furthermore, we show how inclusion of the optimal resource allocation (OA) model can help predict the direction and outcome of PSFs under environmental change.
  2. Plants and associated soil microbes have co-evolved for millennia, generating adaptations to each other and to their local environment. This local co-adaptation is likely generated by a suite of multidirectional exchanges of goods and services among plants, fungi and bacteria, and the constant changes in above-ground–below-ground interactions.
  3. Resource limitation may be a driver of local adaptation among organisms involved in nutritional symbioses. The OA model states that when an essential resource is limited, natural selection will favour taxa that forage optimally by adjusting their biomass and energy allocation such that productivity is equally limited by all resources. Co-adaptation will therefore respond to the local limiting resource conditions through taxa-specific resource transfer interactions.
  4. The OA model can help predict the outcomes of PSFs across a range of resource gradients and environmental changes such as increasing drought or atmospheric nitrogen deposition. Positive feedback is predicted in systems where resource exchange among plants and associated soil microbes can ameliorate resource limitation, or in systems where microbes provide another important service such as pathogen defence. Feedback strength is expected to diminish as resources become less limiting. Negative feedback is predicted when resources are in luxury supply and populations of opportunistic plant pathogens increase relative to commensal or mutualist microbes.
  5. Future, field-based studies that integrate naturally co-occurring systems of plants, microbes and their local soil are needed to further test the hypothesis that resource availability is an effective predictor of the direction and magnitude of PSFs. A more mechanistic understanding of PSFs will help land managers and farmers to manipulate plant–microbial soil interactions to respond to environmental change and to effectively harness beneficial symbioses for plant nutrition and pathogen control.