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Impact of plant-microbial symbioses on global biogeochemical cycling and climate through Earth's history

Dr Katie Field (SOB), Dr Benjamin Mills (SEE), Dr Sarah Batterman (Geo)

Contact email: k.field@leeds.ac.uk

Project background:

Earth’s climate has undergone a number of major shifts over the past 540 million years (the Phanerozoic Eon), yet it is unclear the degree to which these changes were due to the evolution and spread of plants in symbiosis with microorganisms. This PhD project will use a combination of lab-based experimentation, targeted field sampling and mathematical models to provide a first evaluation of the role of plant symbioses in global biogeochemical cycles and climate throughout earth’s history, and their potential impacts on future climate change.

Fig 1. (a) Land plant phylogeny showing divergence of major land plant lineages and (b) coincident changes in atmospheric CO2 concentration across the Palaeozoic (from Field et al., 2012)

One of the most significant climate shifts in Earth’s history was the substantial increase in oxygen to ‘breathable’ levels around 420-400 million years ago (Ma). Coincident with these increasing levels of O2­, atmospheric CO2 concentrations underwent a dramatic decline, falling >90% from 410–340 Ma. This decline is thought to have been driven, in large part, by geochemical weathering processes and by the increasing plant demand for CO2 for photosynthesis. Changes in atmospheric CO2 concentrations have influenced the warming and cooling of climate, and this reduction appears to have lowered global surface temperatures sufficiently to cause a multimillion year ‘ice-age’ during the Permo-Carboniferous. During the Palaeozoic, the terrestrial flora underwent rapid expansion and diversification (Fig. 1), with plants evolving in structural complexity and stature.  The co-evolution of plant rooting systems and symbiotic microbes are likely to have played a crucial role in providing the expanding biomass of terrestrial ecosystems with soil nutrients. This would have become particularly critical as mineral phosphorus (P) sources were depleted.

We now know that the diversity of microorganisms forming mutualistic symbioses with early land plants is likely to have been much greater than previously thought. The recent discovery that the earliest diverging lineages of liverworts (themselves being the earliest diverging lineage of extant land plants) form nutritional symbioses with partially saprotrophic Mucoromycotina fungi brings into question the widely-held assumption that the first land plants formed mutualisms only with arbuscular mycorrhiza-forming fungi of the Glomeromycota. Lab experiments have shown that there are fundamental differences between liverwort-Mucoromycotina and liverwort-Glomeromycota symbioses in their functioning (in terms of carbon-for-nutrient exchange between plants and fungi) and that each type of symbiosis responds differently to changes in atmospheric CO2 concentration.

Moving towards the present day, three recent advances suggest that the evolution of plants in symbiosis with nitrogen fixing bacteria may have had a key feedback with global climate: 1) the pinpointing of the first evolutionary event of plants in symbiosis with nitrogen-fixing bacteria, predominately in the Legume family, around 58 million years ago that coincided with a second major drop in global atmospheric CO2; 2) discovery of the important functional role of nitrogen-fixing plants during periods of rapid carbon accumulation in terrestrial systems by providing large quantities of new nitrogen (N) to ecosystems; and, 3) the potential stimulation of fixation by elevated CO2.

The differences in microbial symbiont CO2 responsiveness in provisioning plant hosts with N and P suggests that plant symbiont identity may have played a greater role in climate modulation that previously thought.  Currently, our knowledge of the drivers of change in Earth’s past climates are based on dynamic global vegetation and climate models (Fig 2 a,b). These have previously been developed and parameterised using data from a variety of sources, including extant land plant responses to simulated past climates. However, none of the existing models take into account the effect of the co-evolution of plants with a variety of microbial symbionts and the critical role they are likely to have played in nutrient cycling and biological weathering throughout the evolution of the terrestrial biosphere.  This project will address this fundamental knowledge gap using a multi-scale approach, using lab experiments, field studies and the development of improved vegetation and climate models to test the following key questions:

  • How did land plants respond to global cooling and CO2 changes in terms of symbiotic function and palaeoecology?
  • To what degree was diversification of land plants and symbiotic partners responsible for past changes in atmospheric O2 and CO2 concentrations?
  • What can we learn from plant evolution and feedbacks with global climate to inform future climate change mitigation strategies?

To address these questions, carbon and nutrient fluxes in plants representative of key clades in the land plant phylogeny will be studied. The species selected will encompass changes in plant structural complexity, nutrient acquisition strategy and choice of symbiotic partner(s). Carbon and nutrient fluxes will be examined using microcosm and isotope tracer-based approaches (Fig 2 c,d) in both the lab and field, with potential field sites in Panama and New Zealand. Together, these data will allow development of dynamic global vegetation models (DGVMs) to include nutrient cycling and carbon-for-nutrient exchange. Such models can then be linked with existing earth system models (ESMs) to explore the relationships and feedbacks between terrestrial biosphere evolution and the Earth’s climate.

Fig. 2 (a) Example model of global carbon uptake by bryophytes (Porada et al., 2013). (b) Model predictions for global NPP under simulated Paleozoic climate (Lenton et al., 2016) (c) Carbon-for nutrient exchange experimental microcosm (Field et al. 2015; 2016) (d) Tropical rainforest in Panama where nitrogen fixers are abundant and provide a key ecosystem function by providing the nitrogen needed to support forest carbon uptake (Batterman et al. 2013a).   

Objectives:

1)    Quantify bidirectional exchange of carbon for nutrients between plants and their symbiotic microbial partners (N-fixing bacteria and mycorrhizal fungi) under changing atmospheric CO2 conditions in controlled environments

2)    Examine the role of plants and their symbionts from across the plant phylogeny in natural ecosystems, including the carbon benefits and costs of entering into symbiosis and emergent ecosystem consequences

3)    Develop dynamic global vegetation models parameterised with empirical data collected in Objectives 1 and 2, and use these to investigate the relationships between plant evolution and climate.

Potential for high impact outcome:

This project will address the critical and fundamental knowledge gaps in our understanding of the development of Earth’s terrestrial biosphere and it’s feedbacks on the atmosphere and climate. The highly interdisciplinary nature and novel objectives underpinning this PhD project, and its focus on critical questions relating to the development of Earth’s atmosphere and biosphere mean there is great potential for high-impact academic outputs. Utilising the unique skillset and expertise of the multi-disciplinary supervisory team and facilities across three schools at the University of Leeds, this project represents a unique opportunity to investigate how plants and their microbial symbionts influenced the development of Earth’s atmosphere and biosphere at multiple scales, and how they might continue to do so in the future, in response to climate change. Central to this is understanding how different plant symbioses (i.e. mycorrhizas and N-fixing bacteria) responded to a changing atmosphere.

Training:

The student will be supervised by Dr Katie Field, an ecophysiologist with special interest in mycorrhiza-CO2 interactions and plant evolution; Dr Benjamin Mills, an Earth system modeller who’s research focuses on the processes controlling CO2 and O2 levels; and Dr Sarah Batterman, an ecologist with specialization in plant nutritional strategies, especially nitrogen fixation, and their emergent ecosystem consequences. Details of the supervisors’ work can be found on the respective websites:

Dr. Field (http://www.plants.leeds.ac.uk/people/groups_fie.php),
Dr. Mills (http://www.see.leeds.ac.uk/people/b.mills)
Dr. Batterman (https://www.geog.leeds.ac.uk/people/s.batterman).

The PhD student will acquire skills and become proficient in a variety of lab, field and modelling techniques. These include isotope tracing, plant physiology, experimental design, ecosystem analysis, mathematical modelling, computer programing and analysis of complex datasets using statistical models. The student will have the opportunity to attend and present their research at UK and international meetings throughout the PhD project, e.g. the British Ecological Society meeting, European Geophysical Union, and the International Conference on Mycorrhiza. These meetings will aid with dissemination of findings and develop the student’s presentation skills while providing them with excellent networking opportunities to facilitate their career development.

References

Batterman, S.A., Hedin, L.O., van Breugel, M., Ransijn, J., Craven, D.J., Hall, J.S. (2013a) Key role of symbiotic N2 fixation in tropical forest secondary succession. Nature 502: 224-227

Batterman, S.A., Wurzburger, N., Hedin, L.O. (2013b) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: A test in Inga punctata. Journal of Ecology 101: 1400-1408

Field KJ, Beerling DJ, Bidartondo MI, Rimington WR, Allinson KE, Cameron DD, Duckett JG, Leake JR, Pressel S. (2016) Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline. The ISME Journal. 10: 1514-1526

Field KJ, Pressel SP, Duckett JD, Rimington WR, Bidartondo MI. (2015) Symbiotic options for the conquest of land. Trends in Ecology and Evolution 30(8): 477-486

Field KJ, Rimington, WR, Bidartondo, MI, Allinson, KE, Beerling, DJ, Cameron, DD, Duckett, JG, Leake, JR & Pressel, S. (2015) First evidence of CO2 responsive mutualisms between ancient lineages of plants and fungi of the Mucoromycotina. New Phytologist 205(2): 743-756

Field KJ, Cameron DD, Leake, JR, Tille, S and Beerling, DJ. (2012) Contrasting arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated Palaeozoic CO2 decline. Nature Communications 3:835 doi: 10.1038/ncomms1831

Lavin, M., Herendeen, P.S., Wojciechowski, M.F.  (2005) Evolutionary Rates Analysis of Leguminosae Implicates a Rapid Diversification of Lineages during the Tertiary. Systematic Biology 54:575-594.

Lenton, T. M., Dahl, T. W., Daines, S. J., Mills, B. J. W., Ozaki, K., Saltzman, M. R. & Porada, P. (2016) Earliest land plants created modern levels of atmospheric oxygen. Proceedings of the National Academy of Sciences of the United States of America 113: 9704-9709

Mills, B. J. W., Belcher, C. M., Lenton, T. M. & Newton, R. J. (accepted) A modelling case for high atmospheric oxygen concentrations during the Mesozoic and Cenozoic. Geology.

Porada, P., Weber, B., Elbert, W., Pöschl, U. & Kleidon, A. (2013) Estimating global carbon uptake by lichens and bryophytes with a process-based model. Biogeosciences 10: 6989-7033, doi:10.5194/bg-10-6989-2013

Sheffer, E., Batterman, S. A., Levin, S. A., Hedin, L. O. (2015) Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nature Plants 1: 15182. doi:10.1038/nplants.2015.182

Werner, G.D.A., Cornwell, W.K., Sprent, J.I., Kattge, J., Kiers, E.T. (2014) A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nature Communications 5

 

Related undergraduate subjects:

  • Biology
  • Earth science
  • Ecology
  • Environmental science