Abstract
Bryophytes maintain symbiosis with bacteria influencing the local nutrient budget. Moss bacterial communities are composed of a core microbiome and bacteria recruited from environmental sources. Notably, symbiotic N2-fixing bacteria contribute to the N budget in northern ecosystems through biological nitrogen fixation. This process may be affected by the abundance of diazotrophs and moss nutrient content. We used the abundant moss Racomitrium lanuginosum in a forest tundra and shrub tundra in Northern Quebec, Canada, to investigate the bacterial and diazotrophic communities associated with habitat type using amplicon sequencing of the bacterial 16S rRNA and nifH genes and test whether the moss core microbiome has recruitment from the soil bacteria community. The nifH amplicons and element analysis were used to test the effect of diazotrophic abundance and moss nutrient content on N2-fixation activity estimated by acetylene reduction assays. Moss microbial communities between tundra types hosted similar bacterial diversity but differentially abundant groups and characteristic microbial interaction patterns. The core microbiome of R. lanuginosum is composed of bacteria strongly associated with northern mosses with no significant recruitment from the soil. The relative abundances of dominant diazotrophs are significantly correlated with acetylene reduction rates. In contrast, the moss nutrient content did not significantly drive N2-fixation. The proteobacterial genera Azorhizobium and Rhodomicrobium represent newly reported bacteria associated with N2-fixation rates in the tundra. We identified critical bacterial groups related to moss-bacterial symbiosis and N2-fixation in the forest-tundra transition zone, a changing environment susceptible to climate warming.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The moss vouchers are deposited at the QFA herbarium corresponding to catalogue numbers QFA-637,608 to QFA-637,686. The raw sequences of this study are deposited in the NCBI Sequence Read Archive (SRA) database under the BioProject PRJNA893897. The moss and soil samples are associated with BioSamples SAMN31436785–SAMN31436859 and SAMN31439125– SAMN31439151, respectively. The moss 16S sequences correspond to SRA accessions SRR22028313–SRR22028356, moss nifH sequences to SRR22032306–SRR22032359, and soil 16S sequences to SRR22031903– SRR22031923. For detailed information, see Supplementary Information Table S1. The dataset and scripts for bioinformatic analyses are available from the corresponding author upon request.
References
Ainon H, Tan CJ, Vikineswary S (2006) Biological characterization of Rhodomicrobium vannielii isolated from a Hot Spring at Gadek, Malacca, Malaysia. Malays J Microbiol. https://doi.org/10.21161/mjm.210603
Alcaraz LD, Peimbert M, Barajas HR et al (2018) Marchantia liverworts as a proxy to plants’ basal microbiomes. Sci Rep 8:1–12. https://doi.org/10.1038/s41598-018-31168-0
Alonso-García M, Villarreal Aguilar JC (2022) Bacterial community of reindeer lichens differs between northern and southern lichen woodlands. Can J For Res 12:1–12. https://doi.org/10.1139/cjfr-2021-0272
Alvarenga DO, Rousk K (2021) Indirect effects of climate change inhibit N2 fixation associated with the feathermoss Hylocomium splendens in subarctic tundra. Sci Total Environ 795:148676. https://doi.org/10.1016/j.scitotenv.2021.148676
Alvarenga DO, Rousk K (2022) Unraveling host–microbe interactions and ecosystem functions in moss–bacteria symbioses. J Exp Bot 73:4473–4486. https://doi.org/10.1093/jxb/erac091
Angel R, Nepel M, Panhölzl C et al (2018) Evaluation of primers targeting the Diazotroph Functional Gene and Development of NifMAP – a Bioinformatics Pipeline for analyzing nifH Amplicon Data. Front Microbiol 9:1–15. https://doi.org/10.3389/fmicb.2018.00703
Aschenbrenner IA, Cernava T, Erlacher A et al (2017) Differential sharing and distinct co-occurrence networks among spatially close bacterial microbiota of bark, mosses and lichens. Mol Ecol 26:2826–2838. https://doi.org/10.1111/mec.14070
Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351. https://doi.org/10.1038/ismej.2011.119
Bay G, Nahar N, Oubre M et al (2013) Boreal feather mosses secrete chemical signals to gain nitrogen. New Phytol 200:54–60. https://doi.org/10.1111/nph.12403
Bell-Doyon P, Bellavance V, Bélanger L et al (2022) Bacterial, fungal, and Mycorrhizal Communities in the Soil Differ between Clearcuts and Insect Outbreaks in the Boreal Forest 50 years after disturbance. SSRN Electron J 4:1–55. https://doi.org/10.2139/ssrn.4140847
Bellenger JP, Darnajoux R, Zhang X, Kraepiel AML (2020) Biological nitrogen fixation by alternative nitrogenases in terrestrial ecosystems: a review. Biogeochemistry 149:53–73. https://doi.org/10.1007/s10533-020-00666-7
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:1–14. https://doi.org/10.3389/fmicb.2014.00219
Bouchard R, Peñaloza-Bojacá G, Toupin S et al (2020) Contrasting bacteriome of the hornwort Leiosporoceros dussii in two nearby sites with emphasis on the hornwort-cyanobacterial symbiosis. Symbiosis 81:39–52. https://doi.org/10.1007/s13199-020-00680-1
Bragina A, Berg C, Berg G (2015) The core microbiome bonds the Alpine bog vegetation to a transkingdom metacommunity. Mol Ecol 24:4795–4807. https://doi.org/10.1111/mec.13342
Brooks ME, Kristensen K, Benthem, Koen JV et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized Linear mixed modeling. R J 9:378. https://doi.org/10.32614/RJ-2017-066
Calabria LM, Petersen KS, Bidwell A, Hamman ST (2020) Moss-cyanobacteria associations as a novel source of biological N2-fixation in temperate grasslands. Plant Soil 456:307–321. https://doi.org/10.1007/s11104-020-04695-x
Callahan B (2018) Silva taxonomic training data formatted for DADA2 (Silva version 132)
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643. https://doi.org/10.1038/ismej.2017.119
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: Architecture and applications. BMC Bioinformatics 10:1–9. https://doi.org/10.1186/1471-2105-10-421
Carella P, Schornack S (2018) Manipulation of Bryophyte hosts by pathogenic and symbiotic microbes special issue. - Rev 0:1–10. https://doi.org/10.1093/pcp/pcx182
Carrell AA, Kolton M, Glass JB et al (2019) Experimental warming alters the community composition, diversity, and N2 fixation activity of peat moss (Sphagnum fallax) microbiomes. Glob Chang Biol 25:2993–3004. https://doi.org/10.1111/gcb.14715
Chapin FS III, Jefferies RL, Reynolds JF et al (1992) Arctic Ecosystems in a Changing Climate, 1st editio. Academic Press. Elsevier
Chen J, Bittinger K, Charlson ES et al (2012) Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28:2106–2113. https://doi.org/10.1093/bioinformatics/bts342
Choudhary S, Blaud A, Osborn AM et al (2016) Nitrogen accumulation and partitioning in a high Arctic tundra ecosystem from extreme atmospheric N deposition events. Sci Total Environ 554–555:303–310. https://doi.org/10.1016/j.scitotenv.2016.02.155
Cutler N (2011) Nutrient limitation during long-term ecosystem development inferred from a mat-forming moss. Bryologist 114:204–214. https://doi.org/10.1639/0007-2745.114.1.204
Daniëls FJa, Gillespie LJ, Poulin M et al (2013) Plants
Darnajoux R, Magain N, Renaudin M et al (2019) Molybdenum threshold for ecosystem scale alternative vanadium nitrogenase activity in boreal forests. Proc Natl Acad Sci 116:201913314. https://doi.org/10.1073/pnas.1913314116
Davis NM, Proctor DiM, Holmes SP et al (2018) Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6:1–14. https://doi.org/10.1186/s40168-018-0605-2
de Jesús Suárez-Moo P, Vovides AP, Patrick Griffith M et al (2019) Unlocking a high bacterial diversity in the coralloid root microbiome from the cycad genus Dioon. PLoS ONE 14:1–20. https://doi.org/10.1371/journal.pone.0211271
DeLuca TH, Zackrisson O, Nilsson MC, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917–920. https://doi.org/10.1038/nature01051
Eddy SR (2011) Accelerated Profile HMM searches. PLOS Comput Biol 7:e1002195. https://doi.org/10.1371/JOURNAL.PCBI.1002195
Edgar RC, Bateman A (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/BIOINFORMATICS/BTQ461
Escolástico-Ortiz DA, Hedenäs L, Quandt D et al (2023) Cryptic speciation shapes the biogeographic history of a northern distributed moss. Bot J Linn Soc 201:114–134. https://doi.org/10.1093/botlinnean/boac027
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Faust K, Raes J (2016) CoNet app: inference of biological association networks using Cytoscape. https://doi.org/10.12688/f1000research.9050.1. F1000Research 5:1519
Frank IE, Turk-Kubo KA, Zehr JP (2016) Rapid annotation of nifH gene sequences using classification and regression trees facilitates environmental functional gene analysis. Environ Microbiol Rep 8:905–916. https://doi.org/10.1111/1758-2229.12455
Gentili F, Nilsson MC, Zackrisson O et al (2005) Physiological and molecular diversity of feather moss associative N2-fixing cyanobacteria. J Exp Bot 56:3121–3127. https://doi.org/10.1093/jxb/eri309
Gordon C, Wynn JM, Woodin SJ (2001) Impacts of increased nitrogen supply on high Arctic heath: the importance of bryophytes and phosphorus availability. New Phytol 149:461–471. https://doi.org/10.1046/j.1469-8137.2001.00053.x
Grace J, Berninger F, Nagy L (2002) Impacts of climate change on the tree line. Ann Bot 90:537–544. https://doi.org/10.1093/aob/mcf222
Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The Acetylene - Ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207
Hare FK, Ritchie JC (1972) The Boreal Bioclimates. Geogr Rev 62:333. https://doi.org/10.2307/213287
Harwood CS (2020) Iron-only and Vanadium Nitrogenases: fail-safe enzymes or something more? Annu Rev Microbiol 74:247–266. https://doi.org/10.1146/annurev-micro-022620-014338
Hedenäs L (2020) Cryptic speciation revealed in Scandinavian Racomitrium lanuginosum (hedw.) Brid. (Grimmiaceae). J Bryol 42:117–127. https://doi.org/10.1080/03736687.2020.1722923
Hodgetts N (2019) Racomitrium lanuginosum. In: IUCN Red List Threat. Species 2019. https://www.iucnredlist.org/species/85844273/87795587
Holland-Moritz H, Stuart J, Lewis LR et al (2018) Novel bacterial lineages associated with boreal moss species. Environ Microbiol 20:2625–2638. https://doi.org/10.1111/1462-2920.14288
Holland-Moritz H, Stuart JEM, Lewis LR et al (2021) The bacterial communities of alaskan mosses and their contributions to N2-fixation. Microbiome 9:53. https://doi.org/10.1186/s40168-021-01001-4
Jean M, Holland-Moritz H, Melvin AM et al (2020) Experimental assessment of tree canopy and leaf litter controls on the microbiome and nitrogen fixation rates of two boreal mosses. New Phytol 227:1335–1349. https://doi.org/10.1111/nph.16611
Jean M, Fenton NJ, Bergeron Y, Nilsson MC (2021) Sphagnum and feather moss-associated N2 fixation along a 724-year chronosequence in eastern boreal Canada. Plant Ecol 222:1007–1022. https://doi.org/10.1007/s11258-021-01157-x
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Klarenberg IJ, Keuschnig C, Russi Colmenares AJ et al (2021) Long-term warming effects on the microbiome and nifH gene abundance of a common moss species in sub‐Arctic tundra. New Phytol. https://doi.org/10.1111/nph.17837
Klarenberg IJ, Keuschnig C, Salazar A et al (2023) Moss and underlying soil bacterial community structures are linked to moss functional traits. Ecosphere 14:1–16. https://doi.org/10.1002/ecs2.4447
Kostka JE, Weston DJ, Glass JB et al (2016) The Sphagnum microbiome: new insights from an ancient plant lineage. New Phytol 211:57–64. https://doi.org/10.1111/nph.13993
Kulichevskaya IS, Ivanova AO, Baulina OI et al (2008) Singulisphaera acidiphila gen. nov., sp. nov., a non-filamentous, Isosphaera-like planctomycete from acidic northen wetlands. Int J Syst Evol Microbiol 58:1186–1193. https://doi.org/10.1099/ijs.0.65593-0
Kulichevskaya IS, Suzina NE, Liesack W, Dedysh SN (2010) Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the acidobacteria. Int J Syst Evol Microbiol 60:301–306. https://doi.org/10.1099/ijs.0.013250-0
Lahti L, Shetty S (2017) Tools for microbiome analysis in R
Lajoie G, Kembel SW (2021) Host neighborhood shapes bacterial community assembly and specialization on tree species across a latitudinal gradient. Ecol Monogr 91. https://doi.org/10.1002/ecm.1443
Larraín J, Quandt D, Stech M, Muñoz J (2013) Lumping or splitting? The case of Racomitrium (Bryophytina: Grimmiaceae). Taxon 62:1117–1132. https://doi.org/10.12705/626.45
Larsson J (2022) eulerr: Area-Proportional Euler and Venn Diagrams with Ellipses
Lee KB, De Backer P, Aono T et al (2008) The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571. BMC Genomics 9:1–14. https://doi.org/10.1186/1471-2164-9-271
Leppänen SM, Salemaa M, Smolander A et al (2013) Nitrogen fixation and methanotrophy in forest mosses along a N deposition gradient. Environ Exp Bot 90:62–69. https://doi.org/10.1016/j.envexpbot.2012.12.006
Ma B, Wang Y, Ye S et al (2020) Earth microbial co-occurrence network reveals interconnection pattern across microbiomes. Microbiome 8:1–12. https://doi.org/10.1186/s40168-020-00857-2
Madigan M, Cox SS, Stegeman RA (1984) Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae. J Bacteriol 157:73–78. https://doi.org/10.1128/jb.157.1.73-78.1984
McMurdie PJ, Holmes S (2013) Phyloseq: an R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217
Morrow MA, Pold G, DeAngelis KM (2020) Draft genome sequence of a terrestrial planctomycete, Singulisphaera sp. Strain GP187, isolated from Forest Soil. Microbiol Resour Announc 9:18–20. https://doi.org/10.1128/MRA.00956-20
Murray MG, Thompson WF (1980) Research Rapid isolation of high molecular weight plant DNA. Nucleic Acids 8:4321–4325
Oksanen J, Blanchet FG, Friendly M et al (2018) vegan: Community Ecology Package
Payette S (1993) The range limit of boreal tree species in Québec-Labrador: an ecological and palaeoecological interpretation. Rev Palaeobot Palynol 79:7–30. https://doi.org/10.1016/0034-6667(93)90036-T
Payette S, Fortin M-J, Gamache I (2001) The Subarctic Forest–Tundra: The Structure of a Biome in a Changing Climate. Bioscience 51:709–718. https://doi.org/10.1641/0006-3568(2001)051[0709:TSFTTS]2.0.CO;2
Prairie Climate Centre, University of Winnipeg (2022) Climate Atlas of Canada. In: Mean Temp. (Annual). Munic. Kuujjuarapik. https://climateatlas.ca/map/canada/annual_meantemp_2030_85#z=8&lat=54.88&lng=-77.47&city=25. Accessed 30 Nov 2022
Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:D501–D504. https://doi.org/10.1093/NAR/GKI025
R Core Team (2017) R Development Core Team. R a Lang. Environ. Stat Comput 55:275–286
Renaudin M, Blasi C, Bradley RL, Bellenger J (2022a) New insights into the drivers of moss-associated nitrogen fixation and cyanobacterial biomass in the eastern canadian boreal forest. J Ecol 102:1–3. https://doi.org/10.1111/1365-2745.13881
Renaudin M, Laforest-Lapointe I, Bellenger J (2022b) Unraveling global and diazotrophic bacteriomes of boreal forest floor feather mosses and their environmental drivers at the ecosystem and at the plant scale in North America. Sci Total Environ 837:155761. https://doi.org/10.1016/j.scitotenv.2022.155761
Rodríguez-Rodríguez JC, Bergeron Y, Kembel SW, Fenton NJ (2022) Dominance of coniferous and broadleaved trees drives bacterial associations with boreal feather mosses. Environ Microbiol 24:3517–3528. https://doi.org/10.1111/1462-2920.16013
Rousk K (2022) Biotic and abiotic controls of nitrogen fixation in cyanobacteria–moss associations. New Phytol 1330–1335. https://doi.org/10.1111/nph.18264
Rousk K, Rousk J (2020) The responses of moss-associated nitrogen fixation and belowground microbial community to chronic Mo and P supplements in subarctic dry heaths. Plant Soil 451:261–276. https://doi.org/10.1007/s11104-020-04492-6
Rousk K, Jones DL, DeLuca TH (2013) Moss-cyanobacteria associations as biogenic sources of nitrogen in boreal forest ecosystems. Front Microbiol 4:1–10. https://doi.org/10.3389/fmicb.2013.00150
Rousk K, Degboe J, Michelsen A et al (2017a) Molybdenum and phosphorus limitation of moss-associated nitrogen fixation in boreal ecosystems. New Phytol 214:97–107. https://doi.org/10.1111/nph.14331
Rousk K, Sorensen PL, Michelsen A (2017b) Nitrogen fixation in the high Arctic: a source of ‘new’. nitrogen? Biogeochemistry 136:213–222. https://doi.org/10.1007/s10533-017-0393-y
Rzepczynska AM, Michelsen A, Olsen MAN, Lett S (2022) Bryophyte species differ widely in their growth and N2 -fixation responses to temperature. Arct Sci. https://doi.org/10.1139/as-2021-0053
Schliep KP (2011) phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593. https://doi.org/10.1093/bioinformatics/btq706
Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/GB-2011-12-6-R60
Shade A, Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14:4–12. https://doi.org/10.1111/j.1462-2920.2011.02585.x
Shannon P, Markiel A, Ozier O et al (2003) Cytoscape: a Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stech M, Veldman S, Larraín J et al (2013) Molecular Species Delimitation in the Racomitrium canescens Complex (Grimmiaceae) and implications for DNA barcoding of Species Complexes in Mosses. PLoS ONE 8. https://doi.org/10.1371/journal.pone.0053134
Stuart JEM, Holland-Moritz H, Lewis LR et al (2021) Host identity as a driver of Moss-Associated N2 fixation rates in Alaska. Ecosystems 24:530–547. https://doi.org/10.1007/s10021-020-00534-3
Sylvain F, Normandeau E, Holland A et al (2022) Genomics of Serrasalmidae teleosts through the lens of microbiome fingerprinting. Mol Ecol 31:4656–4671. https://doi.org/10.1111/mec.16574
Trant AJ, Hermanutz L (2014) Advancing towards novel tree lines? A multispecies approach to recent tree line dynamics in subarctic alpine Labrador, northern Canada. J Biogeogr 41:1115–1125. https://doi.org/10.1111/jbi.12287
Ullrich SR, Poehlein A, Voget S et al (2015) Permanent draft genome sequence of Acidiphilium sp. JA12-A1. Stand Genomic Sci 10. https://doi.org/10.1186/s40793-015-0040-y
Villarreal A, JC, Renaudin M, Beaulieu-Laliberté A, Bellenger JP (2021) Stigonema associated with boreal Stereocaulon possesses the alternative vanadium nitrogenase. Lichenol 53:215–220. https://doi.org/10.1017/S0024282921000062
Vitt DH, Marsh C (1988) Population variation and phytogeography of Racomitrium lanuginosum and R. pruinosum. Beih zur Nov Hedwigia 90:235–260
Wang Q, Quensen JF, Fish JA et al (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using framebot, a new informatics tool. https://doi.org/10.1128/MBIO.00592-13/SUPPL_FILE/MBO005131620S1.PDF. MBio 4:
Ward LM, Cardona T, Holland-Moritz H (2019) Evolutionary implications of Anoxygenic Phototrophy in the bacterial phylum Candidatus Eremiobacterota (WPS-2). Front Microbiol 10:1–12. https://doi.org/10.3389/fmicb.2019.01658
Warshan D, Bay G, Nahar N et al (2016) Seasonal variation in nifH abundance and expression of cyanobacterial communities associated with boreal feather mosses. ISME J 10:2198–2208. https://doi.org/10.1038/ismej.2016.17
Warshan D, Espinoza JL, Stuart RK et al (2017) Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant-cyanobacteria symbiosis. ISME J 11:2821–2833. https://doi.org/10.1038/ismej.2017.134
Weiss S, Van Treuren W, Lozupone C et al (2016) Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J 10:1669–1681. https://doi.org/10.1038/ismej.2015.235
Williams RJ, Howe A, Hofmockel KS (2014) Demonstrating microbial co-occurrence pattern analyses within and between ecosystems. Front Microbiol 5:1–10. https://doi.org/10.3389/fmicb.2014.00358
Wright ES (2016) Using DECIPHER v2.0 to analyze big biological sequence data in R. R J 8:352. https://doi.org/10.32614/RJ-2016-025
Zhang X, McRose DL, Darnajoux R et al (2016) Alternative nitrogenase activity in the environment and nitrogen cycle implications. Biogeochemistry 127:189–198. https://doi.org/10.1007/s10533-016-0188-6
Acknowledgements
We thank the Center of Northern Studies (CEN) for the facilities provided in Kuujuarapik and Umiujaq. In addition, we would like to thank the Bellenger Lab for all the help with N2-fixation experiments, especially Ayan Ibrahim, for her valuable help with the moss element analyses. We want to acknowledge the help of Kim Damboise and Catherine Boudreault in the fieldwork and the provided photographs of the study site. Finally, we thank the two anonymous reviewers for their valuable comments on improving the manuscript.
Funding
This study received financing from fellowships awarded to DAEO (Fonds de recherche du Québec –Nature et technologies through the Merit scholarship program for foreign students (PBEEE) and the Mexican National Council for Science and Technology (CONACYT) through a partial doctoral fellowship), the Discovery Grant (NSERC): RGPIN-2016-05967 and the Canadian Foundation for Innovation (CFI): 39135.
Author information
Authors and Affiliations
Contributions
The study and sampling design was conceived by JCVA, ND and DAEO. Sampling, molecular lab work and data analyses were performed DAEO. Acetylene reduction assays and element analyses were carried out by CB, JPB and DAEO. DAEO wrote the first version of the manuscript with the help of all authors. All authors read and agreed on the final version of the manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Escolástico-Ortiz, D.A., Blasi, C., Bellenger, JP. et al. Differentially abundant bacteria drive the N2-fixation of a widespread moss in the forest-tundra transition zone. Symbiosis 90, 193–211 (2023). https://doi.org/10.1007/s13199-023-00930-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-023-00930-y