The Boreal Nitrogen Gap
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Filling the Boreal Nitrogen Gap: outcomes after three years of research

9/14/2015

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María Arróniz Crespo, Davey L. Jones, Nick Ostle, and Thomas H. DeLuca

Odd though it may seem for this cold and often snowy land, fire is a fundamental feature of the Boreal Forest. The apparent destruction of such a disturbance event is in fact an act of renewal, creating wildlife habitat and maintaining forest health. But fire also opens new dilemmas around nitrogen availability in the boreal forest.  About 250 – 450 kg N ha-1 of this precious nutrient are volatilize in each forest fire, from the burning of needles, twigs, shrubs, and the forest floor.  If N is to be sustained in these forests, N must be replenished within the natural fire return interval.

During the past decades ecologists has been asking the same question over and over again, where does the N come from in a forest without leguminous or woody N fixers? In 2002, Tom DeLuca and colleagues discover that a substantial amount of N can enter the system via biological N fixation in cyanobacteria living epiphytically on feather mosses that cover the forest floor. This finding opened new questions about N dynamics within the boreal ecosystem: Is the fixed N held in the moss? How is all that N transferred ultimately to the trees, and how long is that process taken? and, is there a relationship between forest N status and N fixation rates in the feather mosses? In summary, how all that system works? After three years of intense and exciting research, our research team has generated some remarkable results that we believe will open new ways to understand ecosystem function in the Boreal Forest. The following provides a brief summary of some of our conclusions.  

The relationship between cyanobacteria and feather mosses is often considered an association rather than a symbiosis as it is not yet known whether cyanobacterial colonisation is of benefit to the moss.  Our results from a 360-year fire chronosquence in northern Sweden suggest that the transfer of fixed N from cyanobacteria may have little direct impact on P. schreberi function [1] and occurs only under conditions that facilitate high cyanobacterial colonisation and N fixation rates (e.g. early successional stands without a tree canopy). We traced the fate of fixed N at nanoscale level and observed a spatial differentiation for fixed N acquisition by the moss cells where uptake occurs only by photosynthetically active moss cells [2]. This restricts the moss assimilation of fixed N to conditions when cyanobacteria are present in the green living part of the moss [2]. The newly fixed N assimilated by the moss is greatly conserved in the moss tissue and eventual occurs in the humus layer as moss decomposes [3]. On an annual basis, we suggest that disturbance events such as drying-rewetting cycles may serve as short-term drivers to liberate the fixed N from senescent moss tissue [4]. On a long-term basis, our results showed that fire disturbance could serves as a major driver to liberate the N that is fixed by the cyanobacteria and hold in the moss tissue and humus layer [3].
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On the other hand, the highly diverse bacterial and fungal communities that live in association with the moss [5] appear to access the fixed N efficiently and across all sections of the moss shoot, both green and brown sections [2]. Over the same 360-year fire chronosquence we observed a shift in bacteria community composition associated with the moss layer from oligotrophic to copiotrophic bacteria as stand age, reflecting an ameliorating of growth conditions for bacteria where moss N2 fixation is greatest [4]. Heterotrophic organisms which feed on or interact with cyanobacteria within this complex systems called “the bryosphere” - the living and dead parts of the moss layer along with the associated biota- are likely to play a key role in the turnover and cycling of fixed N at an ecosystem level. In this light, we observed a positive correlation between feather moss N2 fixation and ecosystem N accumulation following stand age, as previously described, but also with soil dissolve organic N and gross turnover of inorganic N along the fire chronosequence studied here [6]. Interestingly, rather than a decline in N status over time our findings indicate that the nutrient status of stands approached equilibrium during late secondary succession after fire where moss N2 fixation is greatest [6]. 

All the work accomplished herein could not been possible without the interest, contribution and enthusiasm of our colleagues. We are grateful to Simon Oakley and Kelly Mason (Lancaster University and CEH Lancaster, UK), Jeremy Bougoure, Daniel Murphy and Peta Clode (The University of Western Australia), Lorna Street (Heriot-Watt University, UK), Nick Cutler (Scott Polar Research Institute, UK), Virginia Souza-Egipsy (CSIC, Spain), Olle Zackrisson and Ingela Bergman (Institute for Subarctic Apline Landscape Research), Stephen Clayton Wade (Advanced Microscopy and Bioimaging Institute of Biological), Sarah Chesworth and Gwen Lancashire (Bangor Univeristy). 
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Publication outcomes (in prep):

1. Lorna E. Street, María Arróniz-Crespo, Leopoldo G. Sancho, Simon Oakley, Nick Ostle, Davey L. Jones and Thomas H DeLuca. Interactive effects of nitrogen deposition and nitrogen fixation on Boreal feather moss function. (Plant, Cell and Environment)

2. María Arróniz-Crespo, Jeremy Bougoure, Daniel Murphy, David L. Jones, Virginia Souza-Egipsy, Nick Cutler, Nick Ostle, Peta Clode, Stephen Clayton Wade, Thomas H. DeLuca. Nitrogen fixation in the boreal bryosphere: it takes a village. (Nature Plants)

3. Thomas H. DeLuca, Olle Zackrisson, Marie-Charlotte Nilsson, María Arróniz-Crespo. Tracing the Long-Term Fate of Nitrogen Fixed by Cyanobacteria in Pleurozium schreberi Brid (Mit.) Moss Carpets of Boreal Forests. (Ecosystems)

4. María Arróniz-Crespo, David L. Jones, Nick Ostle, Gwen Lancashire, Thomas H. DeLuca. Significant releases of organic nitrogen from Pleurozium schreberi Brid (Mit.) moss carpets of Boreal Forests: in situ monitoring by microdialysis probes. (Soil Biology & Biochemistry)

5. Nick A. Cutler, María Arróniz-Crespo, Lorna E. Street, David L. Jones, Dominique L. Chaput, Thomas H. DeLuca. Long-term recovery of microbial communities in the boreal bryosphere following fire disturbance (Ecology)

6. María Arróniz-Crespo, David L. Jones, Lorna E. Street, Nick Ostle, Simon Oakley, Olle Zackrisson, Kathrin Rousk, Johannes Rousk, Kelly Mason, Michael Gundale, Thomas H. DeLuca.. Long-term shifts in stand nutrient status through succession in fire-disturbed boreal forest (Functional Ecology)



*Results presented at the Boreal N Gap Workshop celebrated the 23th of March 2015 at Bangor University (Wales, UK)
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BOREAL N GAP WORKSHOP

3/23/2015

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Venue: The Management Centre, Bangor University (Wales, UK)

Programme

10.30 Welcome by Tom DeLuca and Davey Jones 

COFFEE 

Session: N2 fixation (Chair: Tom DeLuca)

11.00 Tom DeLuca (The University of Washington Seattle)   
Nutrient cycling in the boreal forest: An overview and new insights.

11.30 María Arróniz-Crespo (Bangor University)
Fate of biologically-fixed nitrogen in the boreal bryosphere

11.55 Lorna Street (Heriot-Watt University)
Impact of N2 fixation on feather moss physiology 

12.20 Gwen Lancashire (Bangor Univeristy)
Does gender affect cyanobacterial colonisation on Pleurozium schreberi?

12.35 María Arróniz-Crespo (Bangor University)
N releases from the moss mat: importance of disturbance


13.00 LUNCH 

Session: N and C dynamics (Chair: Nick Ostle)

14.15  Davey Jones (Bangor University)
Mycorrhizal associations and organic N in N limited environments

14.30 Nick Cutler (Churchill College)
Microbial communities of the boreal bryosphere  

14:55 Kelly Mason (CEH Lancaster)
Regulation of boreal soil respiration: evidence from a Swedish forest fire chronosequence.

15.20 Simon Oakley (CEH Lancaster)
GHG dynamics in the boreal forest.

15.45  COFFEE

Session: Summary and overview

16.15 Tom DeLuca, Nick Ostle and Davey Jones

19.00  DINNER
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The Micronauts of the Boreal Forest

6/23/2014

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María Arróniz-Crespo
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In 2010 Zoë Lindo and Andrew Gonzalez described a new concept that changed the way we see bryophytes (mosses and related plants). They defined ´the bryosphere´ as a system formed by the living and dead parts of the moss tissue and the diverse community of microorganisms and invertebrates that inhabit the moss: different components that are connected and interact in a complex way. Zoë and Andrew invited us to change the scale on which we observed mosses to understand their role on ecosystems. This post is about the extraordinary journey of the inhabitants of the boreal forest bryosphere in the attempt to understand how this diverse community interacts in terms of N cycling.

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The trip started last summer in Arjeplog, north Sweden, and will finish this autumn in Perth, Western Australia, where samples of the boreal forest bryosphere will be observed under a NanoSIMS: a secondary ion mass spectrometer that works at nanoscale thereby giving the possibility to direct visualization of nutrient flow within cell structures at submicron length scales! Preparation of the samples for NanoSIMS observation was challenging, but thanks to the inestimable help of Jeff Duckett and Silvia Pressel we found a fixation and embedding method that gave good staining of the microbial community, and also preserved the soft tissue of Pleurozium schreberi. The moss and its crew (cynobacteria, heterotrophic bacteria, fungi and unicellular algae) flew from the understory of the boreal forest to Bangor (SENRGY, Wales) and then to Madrid (Servicio de Microscopía Electrónica, ICA-CSIC, Spain) where samples were prepared. Sample preparation was a craft, resulting in wonderful “moss jewellery”! From Madrid, the boreal micronauts crossed Europe again to land in Aberystwyth (Advanced Microscopy and Bioimaging, Wales) where we spent weeks localizing and observing the association between the moss and its widely diverse epiphytic community in great detail using electron microscopy. From Aberystwyth, the crew started its last flight towards the antipodes. In Perth (School of Earth & Environment, UWA) this autumn, we will be able to complete what we already know about the fate of the fixed N within the boreal bryosphere and, therefore, to improve our understanding of the pathways that the N follows once it’s fixed by the cyanobacteria. It´s been a very exciting and wonderful trip; thanks to all for your interest and great contributions!

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Field excursion September 2013

11/11/2013

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_Hi! This is Maria writing after this autumn's fieldtrip in North Sweden. The last time I was that far up in the north was in 2007 when I was doing some research studies in Abisko as part of Gareth Phoenix´s group. At that time I was impressed with the landscape, now I am convinced Scandinavia is an amazing place to do fieldwork, Tom thank you very much for offering me this job!
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_I stayed in Arjeplog over a month living in a yellow Swedish wooden house and working in close collaboration with colleagues from Silvermuseet, with whom I had the opportunity to share expertise and collate scientific knowledge for a better understanding of the boreal forest. Tom arrived the second week and together we set up a new experiment that will help us to describe the fate of the newly fixed nitrogen. We are really excited about the results we are going to get. Setting up was indeed exciting not just due to the questions we are trying to answer but also because it involved collaboration with people from Arjeplog who offered their assistance. We are indebted for their help without which it would have been very difficult to run a 240V AC peristaltic pump for 24 h continuous sampling during 21 days in a remote area in the middle of the boreal forest! that was amazing, thanks!

I read in a very interesting book about bryophytes that the predominance of Pleurozium schreberi in the boreal forest does not result from its better adaptive potential to ecological conditions, but rather from its ability to remove others, like Ptilidium, Ptilium or Dicranum, through competitive interaction by means of a growth strategy orientated towards the fast occupancy of space. If you are a cyanobacteria, this is excellent news since an increasingly large body of literature is pointing towards the high degree of host specificity of these microorganisms, and guess what, they love Pleurozium schreberi  as a substrate for growing! Why? We are still trying to find out. If you are a tree growing in the boreal forest where nitrogen is very limited, this is also very good news. First because these associations represent an important source of new nitrogen to the ecosystem through the process of nitrogen fixation. However we still need to describe how the newly fixed nitrogen is transfered from the moss system to the tree. The results from this fieldtrip will provide the scientific community with new results to try to solve this puzzle. Secondly, it is also recognized that nutrients can be leached from Pleurozium schreberi after disturbance events -for example after membrane damage from desiccation following wet / dry cycles- which may serve as source of nutrients. However our understanding of this process is limited regarding the net impact. This autumn we have run different studies to try to help fill this knowledge gap.

Another interesting discovery of this autumn's fieldtrip was the Sami singer Sofia Jannok and her album Áphi / Wide as Oceans: very much recommended, thanks Ingela! 

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Field Excursion June 2013

3/21/2012

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_There has been a small change in project management over the last few months. Dr. María Arróniz-Crespo has taken over for Lorna Street as the project manager.  Although we were extremely sad to see Lorna go to Sheffield to take up a new project, we are extremely pleased to have Maria join us.  Maria brings a  wealth of bryophyte physiology expertise to our group and also brings a great deal of enthusiasm to the project.
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_In late May and early June of this year, Maria and I returned to the field sites in Northern Sweden to orient her to the project and to continue running ongoing experiments.  During this visit, the weather was extremely warm and sunny, not particularly seasonal for early June at 66o N! We made a number of  interesting observations during this time.  My oldest son, Emil DeLuca, a junior in Chemistry at the University of Montana, joined us a volunteer field assistant.  Emil greatly increased our capacity to collect samples and set up apparatus along the chornosequence.  His background in chemistry was also handy when it came time for sample analyses.   The Nick Ostle group overlapped with us for a few days and continued to conduct trace gas measurements at the chronosequence sites.

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_During our stay, we set out a new study on N recycling in the moss canopy using ionic resins, continued work on the chronosequence in terms of N dynamics, collected the final results on a micronutrient experiment and initiated and perhaps completed a study on colonization of feather mosses by proximity to N2 fixing lichen and crusts.  There appeared to be little or no relationship between proximity of  mosses to crusts and lichen in terms of cyanobacterial colonization or nitrogenase activity. The micronutrient experiment, now in its third year, demonstrated no significant effect of Mo or Fe on N fixation rates with a possible decrease in N2 fixation with Fe addition. Phosphorus stimulated nitrogenase activity in years 1 and 2, but showed little effect in year three (no additional P added).  More to report, but there are papers to write!

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