Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify

Dijkhuizen LW, Brouwer P, Bolhuis H, Reichart G-J, Koppers N, Huettel B, Bolger AM, Li F-W, Cheng S, Liu X, Wong GK-S, et al. (2018)
New Phytologist 217(1): 453-466.

Download
OA 1.55 MB
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Volltext vorhanden für diesen Nachweis
Autor
; ; ; ; ; ; ; ; ; ; ;
Alle
Abstract / Bemerkung
 Dinitrogen fixation by Nostoc azollae residing in specialized leaf pockets supports prolific growth of the floating fern Azolla filiculoides. To evaluate contributions by further microorganisms, the A.filiculoides microbiome and nitrogen metabolism in bacteria persistently associated with Azolla ferns were characterized.  A metagenomic approach was taken complemented by detection of N2O released and nitrogen isotope determinations of fern biomass. Ribosomal RNA genes in sequenced DNA of natural ferns, their enriched leaf pockets and water filtrate from the surrounding ditch established that bacteria of A. filiculoides differed entirely from surrounding water and revealed species of the order Rhizobiales. Analyses of seven cultivated Azolla species confirmed persistent association with Rhizobiales.  Two distinct nearly full-length Rhizobiales genomes were identified in leaf-pocket-enriched samples from ditch grown A. filiculoides. Their annotation revealed genes for denitrification but not N2-fixation. 15N2 incorporation was active in ferns with N. azollae but not in ferns without. N2O was not detectably released from surface-sterilized ferns with the Rhizobiales.  N2-fixing N. azollae, we conclude, dominated the microbiome of Azolla ferns. The persistent but less abundant heterotrophic Rhizobiales bacteria possibly contributed to lowering O2 levels in leaf pockets but did not release detectable amounts of the strong greenhouse gas N2O.
Erscheinungsjahr
Zeitschriftentitel
New Phytologist
Band
217
Ausgabe
1
Seite(n)
453-466
ISSN
PUB-ID

Zitieren

Dijkhuizen LW, Brouwer P, Bolhuis H, et al. Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify. New Phytologist. 2018;217(1):453-466.
Dijkhuizen, L. W., Brouwer, P., Bolhuis, H., Reichart, G. - J., Koppers, N., Huettel, B., Bolger, A. M., et al. (2018). Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify. New Phytologist, 217(1), 453-466. doi:10.1111/nph.14843
Dijkhuizen, L. W., Brouwer, P., Bolhuis, H., Reichart, G. - J., Koppers, N., Huettel, B., Bolger, A. M., Li, F. - W., Cheng, S., Liu, X., et al. (2018). Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify. New Phytologist 217, 453-466.
Dijkhuizen, L.W., et al., 2018. Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify. New Phytologist, 217(1), p 453-466.
L.W. Dijkhuizen, et al., “Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify”, New Phytologist, vol. 217, 2018, pp. 453-466.
Dijkhuizen, L.W., Brouwer, P., Bolhuis, H., Reichart, G.-J., Koppers, N., Huettel, B., Bolger, A.M., Li, F.-W., Cheng, S., Liu, X., Wong, G.K.-S., Pryer, K., Weber, A., Bräutigam, A., Schluepmann, H.: Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify. New Phytologist. 217, 453-466 (2018).
Dijkhuizen, Laura W., Brouwer, Paul, Bolhuis, Henk, Reichart, Gert-Jan, Koppers, Nils, Huettel, Bruno, Bolger, Anthony M., Li, Fay-Wei, Cheng, Shifeng, Liu, Xin, Wong, Gane Ka-Shu, Pryer, Kathleen, Weber, Andreas, Bräutigam, Andrea, and Schluepmann, Henriette. “Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify”. New Phytologist 217.1 (2018): 453-466.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Creative Commons Namensnennung 4.0 International Public License (CC-BY 4.0):
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2018-05-11T09:15:40Z

1 Zitation in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Fern genomes elucidate land plant evolution and cyanobacterial symbioses.
Li FW, Brouwer P, Carretero-Paulet L, Cheng S, de Vries J, Delaux PM, Eily A, Koppers N, Kuo LY, Li Z, Simenc M, Small I, Wafula E, Angarita S, Barker MS, Bräutigam A, dePamphilis C, Gould S, Hosmani PS, Huang YM, Huettel B, Kato Y, Liu X, Maere S, McDowell R, Mueller LA, Nierop KGJ, Rensing SA, Robison T, Rothfels CJ, Sigel EM, Song Y, Timilsena PR, Van de Peer Y, Wang H, Wilhelmsson PKI, Wolf PG, Xu X, Der JP, Schluepmann H, Wong GK, Pryer KM., Nat Plants 4(7), 2018
PMID: 29967517

65 References

Daten bereitgestellt von Europe PubMed Central.


AUTHOR UNKNOWN, 2013
Relationships for estimating N fixation in legumes: incidence for N balance of legume‐based cropping systems in Europe
AUTHOR UNKNOWN, 2015
The RAST Server: rapid annotations using subsystems technology.
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O., BMC Genomics 9(), 2008
PMID: 18261238
Azolla filiculoides as partial replacement for traditional protein supplements in diets for growing‐fattening pigs based on sugar cane juice
AUTHOR UNKNOWN, 1990
Trimmomatic: a flexible trimmer for Illumina sequence data.
Bolger AM, Lohse M, Usadel B., Bioinformatics 30(15), 2014
PMID: 24695404
Azolla domestication towards a biobased economy?
Brouwer P, Brautigam A, Kulahoglu C, Tazelaar AO, Kurz S, Nierop KG, van der Werf A, Weber AP, Schluepmann H., New Phytol. 202(3), 2014
PMID: 24494738
Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer.
Brouwer P, Brautigam A, Buijs VA, Tazelaar AO, van der Werf A, Schluter U, Reichart GJ, Bolger A, Usadel B, Weber AP, Schluepmann H., Front Plant Sci 8(), 2017
PMID: 28408911
Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species.
Cao HX, Schmutzer T, Scholz U, Pecinka A, Schubert I, Vu GT., Front Microbiol 6(), 2015
PMID: 26236284
R hexbin: hexagonal binning routines
AUTHOR UNKNOWN, 2015
Are bacteria the third partner of the Azolla–Anabaena symbiosis?
AUTHOR UNKNOWN, 1991

AUTHOR UNKNOWN, 2010
Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment.
Castelle CJ, Hug LA, Wrighton KC, Thomas BC, Williams KH, Wu D, Tringe SG, Singer SW, Eisen JA, Banfield JF., Nat Commun 4(), 2013
PMID: 23979677
Evaluation of short read metagenomic assembly
AUTHOR UNKNOWN, 2011
R: data.table. CRAN
AUTHOR UNKNOWN, 2014
Dynamics of bacterial communities before and after distribution in a full-scale drinking water network.
El-Chakhtoura J, Prest E, Saikaly P, van Loosdrecht M, Hammes F, Vrouwenvelder H., Water Res. 74(), 2015
PMID: 25732558
Indole‐3‐acetic acid (IAA) production by Arthrobacter species isolated from Azolla
AUTHOR UNKNOWN, 1992

AUTHOR UNKNOWN, 1991
The biochemistry of the metabolic poison propionate 3-nitronate and its conjugate acid, 3-nitropropionate.
Francis K, Smitherman C, Nishino SF, Spain JC, Gadda G., IUBMB Life 65(9), 2013
PMID: 23893873
Life history and laboratory host range of Stenopelmus rufinasus, a natural enemy for Azolla filiculoides in South Africa
AUTHOR UNKNOWN, 1998
Nitrification by plants that also fix nitrogen.
Hipkin CR, Simpson DJ, Wainwright SJ, Salem MA., Nature 430(6995), 2004
PMID: 15229604
Genome-wide association study of Arabidopsis thaliana leaf microbial community.
Horton MW, Bodenhausen N, Beilsmith K, Meng D, Muegge BD, Subramanian S, Vetter MM, Vilhjalmsson BJ, Nordborg M, Gordon JI, Bergelson J., Nat Commun 5(), 2014
PMID: 25382143
Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review
AUTHOR UNKNOWN, 2012
KEGG for representation and analysis of molecular networks involving diseases and drugs.
Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M., Nucleic Acids Res. 38(Database issue), 2009
PMID: 19880382
Hybrid error correction and de novo assembly of single-molecule sequencing reads.
Koren S, Schatz MC, Walenz BP, Martin J, Howard JT, Ganapathy G, Wang Z, Rasko DA, McCombie WR, Jarvis ED, Adam M Phillippy ., Nat. Biotechnol. 30(7), 2012
PMID: 22750884
RNAmmer: consistent and rapid annotation of ribosomal RNA genes.
Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW., Nucleic Acids Res. 35(9), 2007
PMID: 17452365
Fast gapped-read alignment with Bowtie 2.
Langmead B, Salzberg SL., Nat. Methods 9(4), 2012
PMID: 22388286
Molecular characterization of vulnibactin biosynthesis in Vibrio vulnificus indicates the existence of an alternative siderophore.
Tan W, Verma V, Jeong K, Kim SY, Jung CH, Lee SE, Rhee JH., Front Microbiol 5(), 2014
PMID: 24478763
Immunocytochemical localization of nitrogenase in bacteria symbiotically associated with Azolla spp.
Lindblad P, Bergman B, Nierzwicki-Bauer SA., Appl. Environ. Microbiol. 57(12), 1991
PMID: 1785936
Defining the core Arabidopsis thaliana root microbiome.
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL., Nature 488(7409), 2012
PMID: 22859206
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data.
Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF., Genome Biol. 12(5), 2011
PMID: 21595876
Expanding the marine virosphere using metagenomics.
Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R., PLoS Genet. 9(12), 2013
PMID: 24348267
A whole-genome assembly of Drosophila.
Myers EW, Sutton GG, Delcher AL, Dew IM, Fasulo DP, Flanigan MJ, Kravitz SA, Mobarry CM, Reinert KH, Remington KA, Anson EL, Bolanos RA, Chou HH, Jordan CM, Halpern AL, Lonardi S, Beasley EM, Brandon RC, Chen L, Dunn PJ, Lai Z, Liang Y, Nusskern DR, Zhan M, Zhang Q, Zheng X, Rubin GM, Adams MD, Venter JC., Science 287(5461), 2000
PMID: 10731133
Growth of bacteria on 3-nitropropionic acid as a sole source of carbon, nitrogen, and energy.
Nishino SF, Shin KA, Payne RB, Spain JC., Appl. Environ. Microbiol. 76(11), 2010
PMID: 20382807
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST).
Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R., Nucleic Acids Res. 42(Database issue), 2013
PMID: 24293654
Metagenomic islands of hyperhalophiles: the case of Salinibacter ruber.
Pasic L, Rodriguez-Mueller B, Martin-Cuadrado AB, Mira A, Rohwer F, Rodriguez-Valera F., BMC Genomics 10(), 2009
PMID: 19951421
The foliar microbiome.
Penuelas J, Terradas J., Trends Plant Sci. 19(5), 2014
PMID: 24439491
Classification and phylogeny of the cyanobiont Anabaena azollae Strasburger: an answered question?
Pereira AL, Vasconcelos V., Int. J. Syst. Evol. Microbiol. 64(Pt 6), 2014
PMID: 24737795
The Azolla and Anabaena symbiosis: endophyte continuity in the Azolla life cycle is facilitated by epidermal trichomes
AUTHOR UNKNOWN, 1993
Isolation of Agrobacterium sp., strain from the Azolla leaf cavity
AUTHOR UNKNOWN, 1990
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO., Nucleic Acids Res. 41(Database issue), 2012
PMID: 23193283

AUTHOR UNKNOWN, 2013
Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium.
Ran L, Larsson J, Vigil-Stenman T, Nylander JA, Ininbergs K, Zheng WW, Lapidus A, Lowry S, Haselkorn R, Bergman B., PLoS ONE 5(7), 2010
PMID: 20628610
The combined structural and kinetic characterization of a bacterial nitronate monooxygenase from Pseudomonas aeruginosa PAO1 establishes NMO class I and II.
Salvi F, Agniswamy J, Yuan H, Vercammen K, Pelicaen R, Cornelis P, Spain JC, Weber IT, Gadda G., J. Biol. Chem. 289(34), 2014
PMID: 25002579
Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF., Appl. Environ. Microbiol. 75(23), 2009
PMID: 19801464
Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis.
Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B., Mol. Plant Microbe Interact. 25(1), 2012
PMID: 21970692
Herbivory eliminates fitness costs of mutualism exploiters.
Simonsen AK, Stinchcombe JR., New Phytol. 202(2), 2014
PMID: 24428169

AUTHOR UNKNOWN, 2000
GNU Parallel: the command‐line power tool
AUTHOR UNKNOWN, 2011
Nitrate and flooding induce NO emissions from soybean nodules
AUTHOR UNKNOWN, 2015
The plant microbiome
AUTHOR UNKNOWN, 2013
Community structure and metabolism through reconstruction of microbial genomes from the environment.
Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF., Nature 428(6978), 2004
PMID: 14961025

AUTHOR UNKNOWN, 2002

AUTHOR UNKNOWN, 1992
Ggplot2
AUTHOR UNKNOWN, 2011
Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer.
Wrighton KC, Castelle CJ, Wilkins MJ, Hug LA, Sharon I, Thomas BC, Handley KM, Mullin SW, Nicora CD, Singh A, Lipton MS, Long PE, Williams KH, Banfield JF., ISME J 8(7), 2014
PMID: 24621521
Assessment of transfer methods for comparative genomics of regulatory networks in bacteria.
Kılıc S, Erill I., BMC Bioinformatics 17 Suppl 8(), 2016
PMID: 27586594
Environmental genes and genomes: understanding the differences and challenges in the approaches and software for their analyses.
Zepeda Mendoza ML, Sicheritz-Ponten T, Gilbert MT., Brief. Bioinformatics 16(5), 2015
PMID: 25673291

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 29084347
PubMed | Europe PMC

Suchen in

Google Scholar