Revealing the transfer pathways of cyanobacterial-fixed N into the boreal forest through the feather-moss microbiome

María Arróniz-Crespo; Jeremy Bougoure; Daniel V Murphy; Nick A Cutler; Virginia Souza-Egipsy; Dominique L Chaput; Davey L Jones; Nicholas Ostle; Stephen C Wade; Peta L Clode; Thomas H DeLuca

doi:10.3389/fpls.2022.1036258

Revealing the transfer pathways of cyanobacterial-fixed N into the boreal forest through the feather-moss microbiome

Front Plant Sci. 2022 Dec 9:13:1036258. doi: 10.3389/fpls.2022.1036258. eCollection 2022.

Authors

María Arróniz-Crespo^{1

2}, Jeremy Bougoure³, Daniel V Murphy^{3

4

5}, Nick A Cutler^{6

7}, Virginia Souza-Egipsy⁸, Dominique L Chaput⁹, Davey L Jones^{1

5}, Nicholas Ostle¹⁰, Stephen C Wade¹¹, Peta L Clode^{4

12}, Thomas H DeLuca¹³

Affiliations

¹ School of Natural Sciences, Bangor University, Bangor, United Kingdom.
² School of Agricultural Engineering, CEIGRAM, Universidad Politecnica de Madrid, Madrid, Spain.
³ School of Agriculture and Environment, The University of Western Australia, Perth, WA, Australia.
⁴ Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Perth, WA, Australia.
⁵ Centre for Sustainable Farming Systems, Food Futures Institute, Murdoch University, Murdoch, WA, Australia.
⁶ Department of Geography, Scott Polar Research Institute, Cambridge, United Kingdom.
⁷ School of Geography, Politics and Sociology, Newcastle University, Newcastle, United Kingdom.
⁸ Servicio de Microscopıa Electronica, Instituto Ciencias Agrarias CSIC, Madrid, Spain.
⁹ Biosciences, University of Exeter, Exeter, United Kingdom.
¹⁰ Lancaster Environment Centre, Lancaster University, Lancaster, United Kingdom.
¹¹ Advanced Microscopy and Bioimaging, Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdom.
¹² School of Biological Sciences, The University of Western Australia, Perth, WA, Australia.
¹³ Department of Forest Ecosystems & Society, College of Forestry, Oregon State University, Corvallis, OR, United States.

Abstract

Introduction: Biological N₂ fixation in feather-mosses is one of the largest inputs of new nitrogen (N) to boreal forest ecosystems; however, revealing the fate of newly fixed N within the bryosphere (i.e. bryophytes and their associated organisms) remains uncertain.

Methods: Herein, we combined ¹⁵N tracers, high resolution secondary ion mass-spectrometry (NanoSIMS) and a molecular survey of bacterial, fungal and diazotrophic communities, to determine the origin and transfer pathways of newly fixed N₂ within feather-moss (Pleurozium schreberi) and its associated microbiome.

Results: NanoSIMS images reveal that newly fixed N₂, derived from cyanobacteria, is incorporated into moss tissues and associated bacteria, fungi and micro-algae.

Discussion: These images demonstrate that previous assumptions that newly fixed N₂ is sequestered into moss tissue and only released by decomposition are not correct. We provide the first empirical evidence of new pathways for N₂ fixed in feather-mosses to enter the boreal forest ecosystem (i.e. through its microbiome) and discuss the implications for wider ecosystem function.

Keywords: NanoSIMS; Pleurozium schreberi; biological N2 fixation; boreal forest; moss microbiome; moss-cyanobacteria associations; nitrogen cycling.

Abstract

Grants and funding