[en] Biological nitrogen fixation (BNF) by microorganisms associated with cryptogamic covers, such as cyanolichens and bryophytes, is a primary source of fixed nitrogen in pristine, high-latitude ecosystems. On land, low molybdenum (Mo) availability has been shown to limit BNF by the most common form of nitrogenase (Nase), which requires Mo in its active site. Vanadium (V) and iron-only Nases have been suggested as viable alternatives to countering Mo limitation of BNF; however, field data supporting this long-standing hypothesis have been lacking. Here, we elucidate the contribution of vanadium nitrogenase (V-Nase) to BNF by cyanolichens across a 600-km latitudinal transect in eastern boreal forests of North America. Widespread V-Nase activity was detected (∼15–50% of total BNF rates), with most of the activity found in the northern part of the transect. We observed a 3-fold increase of V-Nase contribution during the 20-wk growing season. By including the contribution of V-Nase to BNF, estimates of new N input by cyanolichens increase by up to 30%. We find that variability in V-based BNF is strongly related to Mo availability, and we identify a Mo threshold of ∼250 ng·glichen−1 for the onset of V-based BNF. Our results provide compelling ecosystem-scale evidence for the use of the V-Nase as a surrogate enzyme that contributes to BNF when Mo is limiting. Given widespread findings of terrestrial Mo limitation, including the carbon-rich circumboreal belt where global change is most rapid, additional consideration of V-based BNF is required in experimental and modeling studies of terrestrial biogeochemistry.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Darnajoux, Romain; Princeton University
Magain, Nicolas ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Renaudin, Marie; Université de Sherbrooke
Lutzoni, François; Duke University
Bellenger, Jean-Philippe; Université de Sherbrooke
Zhang, Xinning; Princeton University
Language :
English
Title :
Molybdenum threshold for ecosystem scale alternative vanadium nitrogenase activity in boreal forests
Publication date :
14 November 2019
Journal title :
Proceedings of the National Academy of Sciences of the United States of America
ISSN :
0027-8424
eISSN :
1091-6490
Publisher :
National Academy of Sciences, Washington DC, United States - District of Columbia
Y. Pan, R. A. Birdsey, O. L. Phillips, R. B. Jackson, The structure, distribution, and biomass of the world’s forests. Annu. Rev. Ecol. Evol. Syst. 44, 593–622 (2013).
J. P. Scharlemann, E. V. Tanner, R. Hiederer, V. Kapos, Global soil carbon: Understanding and managing the largest terrestrial carbon pool. Carbon Manag. 5, 81–91 (2014).
C. Giguère-Croteau et al., North America’s oldest boreal trees are more efficient water users due to increased [CO2], but do not grow faster. Proc. Natl. Acad. Sci. U.S.A. 116, 2749–2754 (2019).
B. D. Sigurdsson, J. L. Medhurst, G. Wallin, O. Eggertsson, S. Linder, Growth of mature boreal Norway spruce was not affected by elevated [CO(2)] and/or air temperature unless nutrient availability was improved. Tree Physiol. 33, 1192–1205 (2013).
W. R. Wieder, C. C. Cleveland, W. K. Smith, K. Todd-Brown, Future productivity and carbon storage limited by terrestrial nutrient availability. Nat. Geosci. 8, 441–444 (2015).
S. Zaehle, Terrestrial nitrogen–carbon cycle interactions at the global scale. Philos. Trans. R. Soc. B Biol. Sci. 368, 20130125 (2013).
R. R. Eady, Structure–Function relationships of alternative nitrogenases. Chem. Rev. 96, 3013–3030 (1996).
D. N. L. Menge et al., Why are nitrogen-fixing trees rare at higher compared to lower latitudes? Ecology 98, 3127–3140 (2017).
W. Elbert et al., Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 5, 459–462 (2012).
K. Rousk, D. L. Jones, T. H. Deluca, Moss-cyanobacteria associations as biogenic sources of nitrogen in boreal forest ecosystems. Front. Microbiol. 4, 150 (2013).
K. Rousk, P. L. Sorensen, A. Michelsen, Nitrogen fixation in the high arctic: A source of “new” nitrogen? Biogeochemistry 136, 213–222 (2017).
K. Rousk, P. L. Sorensen, S. Lett, A. Michelsen, Across-habitat comparison of diazotroph activity in the subarctic. Microb. Ecol. 69, 778–787 (2015).
H. K. Wedepohl, The composition of the continental crust. Geochim. Cosmochim. Acta 59, 1217–1232 (1995).
S. S. Perakis, J. C. Pett-Ridge, Nitrogen-fixing red alder trees tap rock-derived nutrients. Proc. Natl. Acad. Sci. U.S.A. 116, 5009–5014 (2019).
A. M. Trierweiler, K. Winter, L. O. Hedin, Rising CO2 accelerates phosphorus and molybdenum limitation of N2-fixation in young tropical trees. Plant Soil 429, 363–373 (2018).
K. A. Dynarski, B. Z. Houlton, Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytol. 217, 1050–1061 (2018).
D. L. McRose, X. Zhang, A. M. L. Kraepiel, F. M. M. Morel, Diversity and activity of alternative nitrogenases in sequenced genomes and coastal environments. Front. Microbiol. 8, 267 (2017).
J.-P. Bellenger, T. Wichard, Y. Xu, A. M. L. Kraepiel, Essential metals for nitrogen fixation in a free-living N2-fixing bacterium: Chelation, homeostasis and high use efficiency. Environ. Microbiol. 13, 1395–1411 (2011).
T. Thiel, B. S. Pratte, Alternative nitrogenases in anabaena variabilis: The role of molybdate and vanadate in nitrogenase gene expression and activity. Adv. Microbiol. 3, 87–95 (2013).
B. Masepohl et al., Regulation of nitrogen fixation in the phototrophic purple bacterium Rhodobacter capsulatus. J. Mol. Microbiol. Biotechnol. 4, 243–248 (2002).
D. A. Betancourt, T. M. Loveless, J. W. Brown, P. E. Bishop, Characterization of diazotrophs containing Mo-independent nitrogenases, isolated from diverse natural environments. Appl. Environ. Microbiol. 74, 3471–3480 (2008).
B. P. Hodkinson et al., Lichen-symbiotic cyanobacteria associated with Peltigera have an alternative vanadium-dependent nitrogen fixation system. Eur. J. Phycol. 49, 11–19 (2014).
N. Magain et al., Species delimitation at a global scale reveals high species richness with complex biogeography and patterns of symbiont association in Peltigera section Peltigera (Lichenized ascomycota: Lecanoromycetes). Taxon 67, 836–870 (2018).
J. Miadlikowska, F. Lutzoni, Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical and large sub-unit nuclear ribosomal DNA data. Int. J. Plant Sci. 161, 925–958 (2000).
R. Darnajoux, J. Constantin, J. Miadlikowska, F. Lutzoni, J.-P. Bellenger, Is vanadium a biometal for boreal cyanolichens? New Phytol. 202, 765–771 (2014).
R. Darnajoux et al., Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: Importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytol. 213, 680–689 (2017).
X. Zhang et al., Alternative nitrogenase activity in the environment and nitrogen cycle implications. Biogeochemistry 127, 189–198 (2016).
M. J. Dilworth, R. R. Eady, R. L. Robson, R. W. Miller, Ethane formation from acetylene as a potential test for vanadium nitrogenase in vivo. Nature 327, 167–168 (1987).
R. Darnajoux, F. Lutzoni, J. Miadlikowska, J.-P. Bellenger, Determination of elemental baseline using peltigeralean lichens from Northeastern Canada (Québec): Initial data collection for long term monitoring of the impact of global climate change on boreal and subarctic area in Canada. Sci. Total Environ. 533, 1–7 (2015).
A. N. Gagunashvili, Ó. S. Andrésson, Distinctive characters of Nostoc genomes in cyanolichens. BMC Genomics 19, 434 (2018).
R. W. F. Hardy, R. D. Holsten, E. K. Jackson, R. C. Burns, The acetylene-ethylene assay for n(2) fixation: Laboratory and field evaluation. Plant Physiol. 43, 1185–1207 (1968).
S. Thomazeau et al., The contribution of sub-saharan african strains to the phylogeny of cyanobacteria: Focusing on the nostocaceae (nostocales, cyanobacteria). J. Phycol. 46, 564–579 (2010).
J.-P. Bellenger, Y. Xu, X. Zhang, F. M. M. Morel, A. M. L. Kraepiel, Possible contribution of alternative nitrogenases to nitrogen fixation by asymbiotic N2-fixing bacteria in soils. Soil Biol. Biochem. 69, 413–420 (2014).
K. Rousk, J. Degboe, A. Michelsen, R. Bradley, J.-P. Bellenger, Molybdenum and phosphorus limitation of moss-associated nitrogen fixation in boreal ecosystems. New Phytol. 214, 97–107 (2017).
M. E. Jean, K. Phalyvong, J. Forest-Drolet, J.-P. Bellenger, Molybdenum and phosphorus limitation of asymbiotic nitrogen fixation in forests of Eastern Canada: Influence of vegetative cover and seasonal variability. Soil Biol. Biochem. 67, 140–146 (2013).
J. Garty, Biomonitoring atmospheric heavy metals with lichens: Theory and application. Crit. Rev. Plant Sci. 20, 309–371 (2001).
S. C. Reed, C. C. Cleveland, A. R. Townsend, Relationships among phosphorus, molybdenum and free-living nitrogen fixation in tropical rain forests: Results from observational and experimental analyses. Biogeochemistry 114, 135–147 (2013).
K. Ininbergs, G. Bay, U. Rasmussen, D. A. Wardle, M. C. Nilsson, Composition and diversity of nifH genes of nitrogen-fixing cyanobacteria associated with boreal forest feather mosses. New Phytol. 192, 507–517 (2011).
R Core Team, R: A language and environment for statistical computing. http://www.rproject.org. Accessed 3 May 2018. (2018).
M. J. Molina, L. T. Molina, Megacities and atmospheric pollution. J. Air Waste Manag. Assoc. 54, 644–680 (2004).
W. H. Schlesinger, E. M. Klein, A. Vengosh, Global biogeochemical cycle of vanadium. Proc. Natl. Acad. Sci. U.S.A. 114, E11092–E11100 (2017).
J. M. Robertson, J. A. Nesbitt, M. B. J. Lindsay, Aqueous- and solid-phase molybdenum geochemistry of oil sands fluid petroleum coke deposits, Alberta, Canada. Chemosphere 217, 715–723 (2019).
T. J. Sullivan et al., Air pollution success stories in the United States: The value of long-term observations. Environ. Sci. Policy 84, 69–73 (2018).
B. Büdel, T. Dulic, T. Darienko, N. Rybalka, T. Friedl, “Cyanobacteria and algae of biological soil crusts” in Biological Soil Crust: An Organizing Principle in Drylands, B. Weber et al., Eds. (Springer, Cham, 2016), pp. 55–80.
C. Zúñiga, D. Leiva, M. Carú, J. Orlando, Substrates of Peltigera lichens as a potential source of cyanobionts. Microb. Ecol. 74, 561–569 (2017).
J. M. Nelson et al., Complete genomes of symbiotic cyanobacteria clarify the evolution of vanadium-nitrogenase. Genome Biol. Evol. 11, 1959–1964 (2019).
D. N. L. Menge et al., Logarithmic scales in ecological data presentation may cause misinterpretation. Nat. Ecol. Evol. 2, 1393–1402 (2018).
