Abies nordmanniana is an economically important tree crop widely used for Christmas tree production. After initial growth in nurseries, seedlings are transplanted to the field. Rhizosphere bacterial communities generally impact the growth and health of the host plant. However, the dynamics of these communities during A. nordmanniana growth in nurseries, and during transplanting, has not previously been addressed. By a 16S rRNA gene amplicon sequencing approach, we characterized the composition and dynamics of bacterial communities in the rhizosphere during early plant growth in field and greenhouse nurseries and for plants transplanted from the greenhouse to the field. Moreover, the N-cycling potential of rhizosphere bacteria across plant age was addressed in both nurseries. Overall, a rhizosphere core microbiome of A. nordmanniana, comprising 19.9% of the taxa at genus level, was maintained across plant age, nursery production systems, and even during the transplantation of plants from the greenhouse to the field. The core microbiome included the bacterial genera Bradyrhizobium, Burkholderia, Flavobacterium, Pseudomonas, Rhizobium, Rhodanobacter, and Sphingomonas, which harbor several N-fixing and plant growth-promoting taxa. Nevertheless, both plant age and production system caused significant changes in the rhizosphere bacterial communities. Concerning community composition, the relative abundance of Rhizobiales (genera Rhizobium, Bradyrhizobium, and Devosia) was higher in the rhizosphere of field-grown A. nordmanniana, whereas the relative abundance of Enterobacteriales and Pseudomonadales (genus Pseudomonas) was higher in the greenhouse. Analysis of community dynamics across plant age showed that in the field nursery, the most abundant bacterial orders showed more dynamic changes in their relative abundance in the rhizosphere than in the bulk soil. In the greenhouse, age-dependent dynamics even occurred but affected different taxa than for the field-grown plants. The N-cycling potential of rhizosphere bacterial communities showed an increase of the relative abundance of genes involved in nitrogen fixation and denitrification by plant age. Similarly, the relative abundance of reported nitrogen-fixing or denitrifying bacteria increased by plant age. However, different community structures seemed to lead to an increased potential for nitrogen fixation and denitrification in the field versus greenhouse nurseries.

Department of Adaptive Biotechnologies Global Change Research Institute CAS Brno Czechia

Department of Plant and Environmental Sciences Faculty of Science University of Copenhagen Frederiksberg Denmark

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Andersen K. S., Kirkegaard R. H., Karst S. M., Albertsen M. (2018). ampvis2: an R package to analyse and visualise 16S rRNA amplicon data.

Anderson C., Beare M., Buckley H. L., Lear G. (2017). Bacterial and fungal communities respond differently to varying tillage depth in agricultural soils. PubMed DOI PMC

Bais H. P., Weir T. L., Perry L. G., Gilroy S., Vivanco J. M. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. PubMed DOI

Bolyen E., Rideout J. R., Dillon M. R., Bokulich N. A., Abnet C. C., Al-Ghalith G. A., et al. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. PubMed DOI PMC

Braga R. M., Dourado M. N., Araújo W. L. (2016). Microbial interactions: ecology in a molecular perspective. PubMed DOI PMC

Bräuner Nielsen U., Hansen J. K., Kromann H. K. (2011). Impact of site and provenance on economic return in Nordmann fir Christmas tree production. DOI

Bürgman H., Meier S., Bunge M., Widmer F., Zeyer J. (2005). Effects of model root exudates on structure and activity of a soil diazotrof community. PubMed DOI

Caliz J., Montes-Borrego M., Triadó-Margarit X., Metsis M., Landa B. B., Casamayor E. O. (2015). Influence of edaphic, climatic, and agronomic factors on the composition and abundance of nitrifying microorganisms in the rhizosphere of commercial olive crops. PubMed DOI PMC

Callahan B. J., McMurdie P. J., Rosen M. J., Han A. W., Johnson A. J. A., Holmes S. P. (2016). DADA2: high-resolution sample inference from Illumina amplicon data. PubMed DOI PMC

Cassman N. A., Leite M. F. A., Pan Y., De Hollander M., Van Veen J. A., Kuramae E. E. (2016). Plant and soil fungal but not soil bacterial communities are linked in long-term fertilized grassland. PubMed DOI PMC

Cernava T., Erlacher A., Soh J., Sensen C. W., Grube M., Berg G. (2019). PubMed DOI PMC

Chaparro J. M., Badri D. V., Vivanco J. M. (2014). Rhizosphere microbiome assemblage is affected by plant development. PubMed DOI PMC

Chu H., Haihua W., Chen H., Tang M. (2016). Pine wilt disease alters soil properties and root-associated fungal communities in DOI

Deng B., Fu L., Zhang X., Zheng J., Peng L., Sun J., et al. (2014). The denitrification characteristics of PubMed DOI PMC

Dennis P. G., Miller A. J., Hirsch P. R. (2010). Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? PubMed DOI

Desjardins P., Conklin D. (2010). NanoDrop microvolume quantitation of nucleic acids. PubMed DOI PMC

Dicenzo G. C., Zamani M., Checcucci A., Fondi M., Griffitts J. S., Finan T. M., et al. (2019). Multidisciplinary approaches for studying rhizobium–legume symbioses. PubMed DOI

Edwards J. A., Santos-Medellín C. M., Liechty Z. S., Nguyen B., Lurie E., Eason S., et al. (2018). Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PubMed DOI PMC

Eichorst S. A., Trojan D., Roux S., Herbold C., Rattei T., Woebken D. (2018). Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. PubMed DOI PMC

Espenberg M., Truu M., Mander Ü., Kasak K., Nõlvak H., Ligi T., et al. (2018). Differences in microbial community structure and nitrogen cycling in natural and drained tropical peatland soils. PubMed DOI PMC

Faith D. P. (1992). Conservation evaluation and phylogenetic diversity. DOI

Garcia-Lemos A. M., Großkinsky D. K., Stokholm M. S., Lund O. S., Nicolaisen M. H., Roitsch T. G., et al. (2019). Root-associated microbial communities of PubMed DOI PMC

Garrido-Oter R., Nakano R. T., Dombrowski N., Ma K. W., McHardy A. C., Schulze-Lefert P. (2018). Modular traits of the rhizobiales root microbiota and their evolutionary relationship with symbiotic rhizobia. PubMed DOI PMC

Gobbi A., Santini R. G., Filippi E., Ellegaard-Jensen L., Jacobsen C. S., Hansen L. H. (2019). Quantitative and qualitative evaluation of the impact of the G2 enhancer, bead sizes and lysing tubes on the bacterial community composition during DNA extraction from recalcitrant soil core samples based on community sequencing and qPCR. PubMed DOI PMC

Haas J. C., Street N. R., Sjödin A., Lee N. M., Högberg M. N., Näsholm T., et al. (2018). Microbial community response to growing season and plant nutrient optimisation in a boreal Norway spruce forest. DOI

Hai B., Diallo N. H., Sall S., Haesler F., Schauss K., Bonzi M., et al. (2009). Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. PubMed DOI PMC

Hardoim P. R., van Overbeek L. S., Berg G., Pirttilä A. M., Compant S., Campisano A., et al. (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. PubMed DOI PMC

Heckman J., Vodak M. (2012).

Henderson S. L., Dandie C. E., Patten C. L., Zebarth B. J., Burton D. L., Trevors J. T., et al. (2010). Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. PubMed DOI PMC

Henry S., Texier S., Hallet S., Bru D., Dambreville C., Chèneby D., et al. (2008). Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. PubMed DOI

Hester E. R., Harpenslager S. F., van Diggelen J. M. H., Lamers L. L., Jetten M. S. M., Lüke C., et al. (2018). Linking nitrogen load to the structure and function of wetland soil and rhizosphere microbial communities. PubMed DOI PMC

Houlden A., Timms-Wilson T. M., Day M. J., Bailey M. J. (2008). Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. PubMed DOI

Igiehon N. O., Babalola O. O. (2018). Rhizosphere microbiome modulators: contributions of nitrogen fixing bacteria towards sustainable agriculture. PubMed DOI PMC

Izumi H., Anderson I. C., Alexander I. J., Killham K., Moore E. R. B. (2006). Endobacteria in some ectomycorrhiza of Scots pine ( PubMed DOI

Karimi B., Dequiedt S., Terrat S., Jolivet C., Arrouays D., Wincker P., et al. (2019). Biogeography of soil bacterial networks along a gradient of cropping intensity. PubMed DOI PMC

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. PubMed DOI PMC

Khetmalas M. B., Egger K. N., Massicotte H. B., Tackaberry L. E., Clapperton M. J. (2002). Bacterial diversity associated with subalpine fir ( PubMed DOI

Kielak A. M., Barreto C. C., Kowalchuk G. A., van Veen J. A., Kuramae E. E. (2016). The ecology of Acidobacteria: moving beyond genes and genomes. PubMed DOI PMC

Kuramae E. E., Yergeau E., Wong L. C., Pijl A. S., van Veen J. A., Kowalchuk G. A. (2012). Soil characteristics more strongly influence soil bacterial communities than land-use type. PubMed DOI

Lareen A., Burton F., Scha P. (2016). Plant root-microbe communication in shaping root microbiomes. PubMed DOI PMC

Lau J. A., Lennon J. T. (2012). Rapid responses of soil microorganisms improve plant fitness in novel environments. PubMed DOI PMC

Li Y., Jia Z., Sun Q., Cheng J., Yang Y., Zhan J., et al. (2017). Plant-mediated changes in soil N-cycling genes during revegetation of copper mine tailings. DOI

Li Y., Jing H., Xia X., Cheung S., Suzuki K., Liu H. (2018). Metagenomic insights into the microbial community and nutrient cycling in the western subarctic Pacific Ocean. PubMed DOI PMC

Lladó S., López-Mondéjar R., Baldrian P. (2017). Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global change. PubMed DOI PMC

Lozupone C., Knight R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. PubMed DOI PMC

Marques J. M., da Silva T. F., Vollu R. E., Blank A. F., Ding G.-C., Seldin L., et al. (2014). Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. PubMed DOI

Marschner P., Crowley D., Yang C. H. (2004). Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. DOI

Mendes L. W., Kuramae E. E., Navarrete A. A., van Veen J. A., Tsai S. M. (2014). Taxonomical and functional microbial community selection in soybean rhizosphere. PubMed DOI PMC

Meng Q., Xu X., Zhang W., Cheng L., Men M., Xu B., et al. (2018). Diversity and abundance of denitrifiers during cow manure composting. PubMed DOI

Mercado-Blanco J., Abrantes I., Caracciolo A. B., Bevivino A., Ciancio A., Grenni P., et al. (2018). Belowground microbiota and the health of tree crops. PubMed DOI PMC

Micallef S. A., Channer S., Shiaris M. P., Colón-Carmona A. (2009). Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. PubMed DOI PMC

Millard P., Grelet G. A. (2010). Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. PubMed DOI

Miller M., Zebarth B., Dandie C., Burton D., Goyer C., Trevors J. (2008). Crop residue influence on denitrification, N2O emissions and denitrifier community abundance in soil. DOI

Miller M., Zebarth B., Dandie C., Burton D., Goyer C., Trevors J. (2009). Influence of liquid manure on soil denitrifier abundance, denitrification, and nitrous oxide emissions. DOI

Na X., Cao X., Ma C., Ma S., Xu P., Liu S., et al. (2019). Plant stage, not drought stress, determines the effect of cultivars on bacterial community diversity in the rhizosphere of broomcorn millet ( PubMed DOI PMC

Na X., Xu T. T., Li M., Ma F., Kardol P. (2017). Bacterial diversity in the rhizosphere of two phylogenetically closely related plant species across environmental gradients. DOI

Naumova N. B., Kuznetsova G. V., Alikina T. Y., Kabilov M. R. (2015). Bacterial 16S DNA diversity in the rhizosphere soil of the two pine species.

Nguyen N. H., Bruns T. D. (2015). The microbiome of PubMed DOI

Niehaus L., Boland I., Liu M., Chen K., Fu D., Henckel C., et al. (2019). Microbial coexistence through chemical-mediated interactions. PubMed DOI PMC

Oliveros J. C. (2007).

Philippot L., Raaijmakers J. M., Lemanceau P., Van Der Putten W. H. (2013). Going back to the roots: the microbial ecology of the rhizosphere. PubMed DOI

Plett J. M., Martin F. M. (2018). Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms. PubMed DOI

Price M. N., Dehal P. S., Arkin A. P. (2010). FastTree 2 - Approximately maximum-likelihood trees for large alignments. PubMed DOI PMC

Proença D. N., Francisco R., Kublik S., Schöler A., Vestergaard G., Schloter M., et al. (2017). The microbiome of endophytic, wood colonizing bacteria from pine trees as affected by pine wilt disease. PubMed DOI PMC

Qin S., Zhang P., Zhou W., Lyu D. (2019). Assessment of species richness and diversity of DOI

Rasmussen H. N., Bjarke Veierskov B., Hansen-Møller J., Nørbaek R. (2009). Cytokinin profiles in the conifer tree DOI

Rodrigues Coelho M. R., De Vos M., Carneiro N. P., Marriel I. E., Paiva E., Seldin L. (2008). Diversity of nifH gene pools in the rhizosphere of two cultivars of sorghum ( PubMed DOI

Roos S., Dicksved J., Tarasco V., Locatelli E., Ricceri F., Grandin U., et al. (2013). 454 pyrosequencing analysis on faecal samples from a randomized DBPC trial of colicky infants treated with PubMed DOI PMC

Rosenberg E., Zilber-Rosenberg I. (2016). Microbes drive evolution of animals and plants: the hologenome concept. PubMed DOI PMC

Rousk J., Baath E., Brookes P. C., Lauber C. L., Lozupone C., Caporaso J. G., et al. (2010). Soil bacterial and fungal communities across a pH gradient in an arable soil. PubMed DOI

Saarenheimo J., Tiirola M. A., Rissanen A. J. (2015). Functional gene pyrosequencing reveals core proteobacterial denitrifiers in boreal lakes. PubMed DOI PMC

Santhanam R., Luu V. T., Weinhold A., Goldberg J., Oh Y., Baldwin I. T. (2015). Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. PubMed DOI PMC

Schlemper T. R., Leite F. A., Lucheta A. R., Shimels M., Bouwmeester H. J., Van Veen J. A., et al. (2017). Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. PubMed DOI

Seifert J. R. (2015). Growing Christmas trees.

Shi C., Wang C., Xu X., Huang B., Wu L., Yang D. (2014). Comparison of bacterial communities in soil between nematode-infected and nematode-uninfected DOI

Sun H., Terhonen E., Koskinen K., Paulin L., Kasanen R., Asiegbu F. O. (2014). Bacterial diversity and community structure along different peat soils in boreal forest. DOI

Tedersoo L., Smith M. E. (2013). Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. DOI

Tveit A., Schwacke R., Svenning M. M., Urich T. (2013). Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. PubMed DOI PMC

Uroz S., Buée M., Deveau A., Mieszkin S., Martin F. (2016). Ecology of the forest microbiome: highlights of temperate and boreal ecosystems. DOI

Vázquez-Baeza Y., Pirrung M., Gonzalez A., Knight R. (2013). EMPeror: a tool for visualizing high-throughput microbial community data. PubMed DOI PMC

Wagner M. R., Lundberg D. S., Del Rio T. G., Tringe S. G., Dangl J. L., Mitchell-Olds T. (2016). Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. PubMed DOI PMC

Wang Q., Quensen J., Fish F., Lee J. A., Kwon T., Tiedje Y., et al. (2013). Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using framebot, a new informatics tool. PubMed DOI PMC

Wang Z., Liu L., Chen Q., Wen X., Liu Y., Han J., et al. (2017). Conservation tillage enhances the stability of the rhizosphere bacterial community responding to plant growth. DOI

Wüst P. K., Horn M. A., Drake H. L. (2011). Clostridiaceae and PubMed DOI PMC

Yang Y., Wang N., Guo X., Zhang Y., Ye B. (2017). Comparative analysis of bacterial community structure in the rhizosphere of maize by high- throughput pyrosequencing. PubMed DOI PMC

Yeoh Y. K., Dennis P. G., Paungfoo-Lonhienne C., Weber L., Brackin R., Ragan M. A., et al. (2017). Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. PubMed DOI PMC

Yoshida M., Ishii S., Otsuka S., Senoo K. (2010). nirk-harboring denitrifiers are more responsive to denitrification-inducing conditions in rice paddy soil than nirs-harboring bacteria. PubMed DOI

Yu H. X., Wang C. Y., Tang M. (2013). Fungal and bacterial communities in the rhizosphere of PubMed DOI PMC

Zhalnina K., Louie K. B., Hao Z., Mansoori N., Da Rocha U. N., Shi S., et al. (2018). Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. PubMed DOI

Identification of Root-Associated Bacteria That Influence Plant Physiology, Increase Seed Germination, or Promote Growth of the Christmas Tree Species Abies nordmanniana