Heterotrophic N2-fixation contributes to nitrogen economy of a common wetland sedge, Schoenoplectus californicus

. 2018 ; 13 (4) : e0195570. [epub] 20180423

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29684035

A survey of the ecological variability within 52 populations of Schoenoplectus californicus (C.A. Mey.) Soják across its distributional range revealed that it is commonly found in nitrogen (N) limited areas, but rarely in phosphorus limited soils. We explored the hypothesis that S. californicus supplements its nitrogen demand by bacterial N2-fixation processes associated with its roots and rhizomes. We estimated N2-fixation of diazotrophs associated with plant rhizomes and roots from several locations throughout the species' range and conducted an experiment growing plants in zero, low, and high N additions. Nitrogenase activity in rhizomes and roots was measured using the acetylene reduction assay. The presence of diazotrophs was verified by the detection of the nifH gene. Nitrogenase activity was restricted to rhizomes and roots and it was two orders of magnitude higher in the latter plant organs (81 and 2032 nmol C2H4 g DW-1 d-1, respectively). Correspondingly, 40x more nifH gene copies were found on roots compared to rhizomes. The proportion of the nifH gene copies in total bacterial DNA was positively correlated with the nitrogenase activity. In the experiment, the contribution of fixed N to the plant N content ranged from 13.8% to 32.5% among clones from different locations. These are relatively high values for a non-cultivated plant and justify future research on the link between N-fixing bacteria and S. californicus production.

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Aerts R, Chapin FS. The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns. Advances in Ecological Research 2000; 30:1–67.

Bedford BL, Walbridge MR, Aldous A. Patterns in nutrient availability and plant diversity of temperate North American wetlands. Ecology 1999; 80:2151–2169.

Vance CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 2003; 157:423–447. PubMed

Ticconi CA, Abel S. Short on phosphate: plant surveillance and countermeasures. Trends in Plant Science 2004; 9:548–555. doi: 10.1016/j.tplants.2004.09.003 PubMed DOI

Rejmánková E, Snyder J. Emergent macrophytes in phosphorus limited marshes: do phosphorus usage strategies change after nutrient addition? Plant and Soil 2008; 313:141–153.

Jurelevicius D, Korenblum E, Casella R, Vital R L, Seldin L. Polyphasic analysis of the bacterial community in the rhizosphere and roots of Cyperus rotundus L. grown in a petroleum-contaminated soil. Journal of Microbiological Biotechnology 2010; 20:862–870 PubMed

Turner TR, James EK, Poole PS. The plant microbiome. Genome Biology 2013; 14:209 doi: 10.1186/gb-2013-14-6-209 PubMed DOI PMC

Weier KL, Pittaway PA, Wildin JH. Role of N2-fixation in the sustainability of the ponded grass pasture system. Soil Biology and Biochemistry 1995; 27:441–445.

Dakora FD, Drake BG. Elevated CO2 stimulates associative N2 fixation in a C3 plant of the Chesapeake Bay wetland. Plant and Cell Environment 2000; 23:943–953.

Bürgmann H, Meier S, Bunge M, Widmer F, Zeyer J. Effects of model root exudates on structure and activity of a soil diazotroph community. Environmental Microbiology 2005; 7:1711–1724 doi: 10.1111/j.1462-2920.2005.00818.x PubMed DOI

Šantrůčková H, Rejmánková E, Pivničková B, Snyder J. Nutrient enrichment in tropical wetlands: shifts from autotrophic to heterotrophic nitrogen fixation. Biogeochemistry 2010; 101:295–310.

Reis VM, dos Reis FB Jr, Quesada DMB, de Oliveira OCA, Alves BJR, Urquiaga S et al. Biological nitrogen fixation associated with tropical pasture grasses. Australian Journal of Plant Physiology 2001; 28:837–844.

de Morais RF, Quesada DM, Reis VM. Contribution of biological N2 fixation to Elephant grass (Pennisetum purpureum Schum.). Plant and Soil 2012; 356:23–34.

Eckard NA, Biesboer DD. A survey of nitrogen fixation (acetylene reduction) associated with Typha in Minnesota. Canadian Journal of Botany 1988; 66:2419–2423.

Wickstrom CE and Corkran JL. Nitrogenase activities associated with macrophytes from a lacustrine and a freshwater estuarine habitat. Aquatic Botany 1997; 59:157–162

Mwaura FB, Widdowson D. Nitrogenase activity in the papyrus swamps of Lake Naivasha, Kenya Hydrobiologia 1992; 232:23–30.

Prakamhang J, Minamisawa K, Teamtaisong K, Boonkerd N, Teaumroong N. The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.). Applied Soil Ecology 2009; 42:141–149.

James EK, Baldani JI. The role of biological nitrogen fixation by non-legumes in the sustainable production of food and biofuels. Plant and Soil 2012; 356:1–3.

Keymer DP, Kent AD. Contribution of nitrogen fixation to first year Miscanthus x giganteus. GCB Bioenergy 2014; 6:577–586.

Knoth JL, Soo-Hyung Kim, Ettl GJ, Doty SL. Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia. New Phytologist 2014; 201:599–609. doi: 10.1111/nph.12536 PubMed DOI

Rosenblueth M, Martínez-Romero E. Bacterial endophytes and their interactions with hosts. Molecular Plant-Microbe Interactions 2006; 19:827–837. doi: 10.1094/MPMI-19-0827 PubMed DOI

Reinhold-Hurek B, Hurek T. Living inside plants: bacterial endophytes. Current Opinion in Plant Biology 2011; 14:435–443. doi: 10.1016/j.pbi.2011.04.004 PubMed DOI

Carpenter HM 2009. Caballitos and Totora: The story of the sedge Schoenoplectus californicus PhD dissertation, University of California, Davis: 2009.

Thullen JS, Nelson SM, Cade BS, Sartoris JJ. Macrophyte decomposition in a surface-flow ammonia-dominated constructed wetland: Rates associated with environmental and biotic variables. Ecological Engineering 2008; 32:281–290.

Dejoux C, Iltis A. Lake Titcaca: a synthesis of limnological knowledge Kluwer Academic Publishers, Boston: 1992.

Rondon XJ, Banack SA, Diaz-Huamanchumo W. Ethnobotanical investigation of caballitos (Schoenoplectus californicus: Cyperaceae) in Huanchaco, Peru. Economic Botany 2003; 57:35–47.

Rejmánková E. Nutrient resorption in wetland macrophytes: comparison across several regions with different nutrient status. New Phytologist 2005; 167:471–482. doi: 10.1111/j.1469-8137.2005.01449.x PubMed DOI

Reich PB, Hungate BA, Luo Y. Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annual Review of Ecology, Evolution and Systematics 2006; 37:611–36.

Reed SC, Cleveland CC, Townsend AR. Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annual Review of Ecology, Evolution and Systematics 2011; 42:489–512.

Vitousek PM, Porder S, Houlton BZ, Chadwick OA. Terrestrial phosphorus limitation: mechanisms, implications and nitrogen-phosphorus interactions. Ecological Application 2010; 20:5–15. PubMed

Santi C, Bogusz D, Franche C. Biological nitrogen fixation in non-legume plants. Annals of Botany 2013; 111:743–767. doi: 10.1093/aob/mct048 PubMed DOI PMC

Reed SC, Cleveland CC, Townsend AR. Relationships among phosphorus, molybdenum and free living nitrogen fixation in tropical rain forests: results from observational and experimental analyses. Biogeochemistry 2013; 114:135–147.

DeLuca TH, Zackrisson O, Nilsson M Ch, Sellstedt A. Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 2002; 419:217–220. PubMed

Boddey RM, de Oliveira OC, Urquiaga S, Reis VM, Olivares FL, Baldani VLD et al. Biological nitrogen fixation associated with sugarcane and rice: contributions and prospects for improvement. Plant and Soil 1995; 174:195–209.

Boddey RM, Urquiaga S, Alves BJR, Reis V. Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant and Soil 2003; 252:139–149.

Haiyambo DH, Chimwamurombe PM, Reinhold-Hurek B. Isolation and screening of rhizosphere bacteria from grasses in East Kavango region of Namibia for plant growth promoting characteristics. Current Microbiology 2015; 71:566–571. doi: 10.1007/s00284-015-0886-7 PubMed DOI

Dalton DA, Kramer S, Azios N, Fusaro S, Cahill E, Kennedy Ch. Endophytic nitrogen fixation in dune grasses (Ammophila arenaria and Elymus mollis) from Oregon. FEMS Microbial Ecology 2004; 49:469–479. PubMed

Terakado-Tonooka J, Fujihara S, Ohwaki Y. Possible contribution of Bradyrhizobium on nitrogen fixation in sweet potatoes. Plant and Soil 2013; 367:639–650.

Rout ME, Chrzanowski TH. The invasive Sorghum halepense harbors endophytic N2-fixing bacteria and alters soil biogeochemistry. Plant and Soil 2009; 315:163–172.

Stal LJ. Nitrogen fixation in cyanobacterial mats. Methods in Enzymology 1988; 167:474–484.

Montoya JP, Voss M, Kähler P, Capone DG. A simple, high-precision, high-sensitivity tracer assay for N2 fixation. Applied Environmental Microbiology 1996; 62:986–993 PubMed PMC

Zehr JP, Montoya JP. Measuring N2 fixation in the field In: Bothe H, Ferguson SJ, Newton WE(eds) Biology of nitrogen cycle. Elsevier B.V, Amsterdam, pp 452 2007.

McNamara AE, Hill WR. UV-B irradiance gradient affects photosynthesis and pigments but not food quality of periphyton. Freshwater Biology 2000; 43:649–662.

Phillips DL, Gregg JW. Uncertainty in source partitioning using stable isotopes. Oecologia 2001; 127:171–179; the mixing model can also be found at (accessed 6.1.2017): https://www.google.com/?ion=1&espv=2#q=ISOERROR+1.04+7%2F20%2F2001+Microsoft+Excel+2000+worksheet+to+accompany%3A). doi: 10.1007/s004420000578 PubMed DOI

Henry S, Baudion E, López-Guitérez JC, Martin-Laurent F, Brauman A, Philippot L. Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. Journal of Microbiological Methods 2004; 59:327–335. doi: 10.1016/j.mimet.2004.07.002 PubMed DOI

Gaby JC, Buckley DH. A Comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLOS ONE 2012; 7:e42149 doi: 10.1371/journal.pone.0042149 PubMed DOI PMC

Sokal R R, Rohlf F J. Biometry 3rd Edition Freeman & Comp; New York: 1995, 887 p.

Asis CA Jr., Shimizu T, Khan MW, Akao S. Organic acid and sugar contents in sugarcane stem apoplast solution and their role as carbon source for endophytic diazotrophs. Soil Science and Plant Nutrition 2003; 49:915–920.

Gyaneshwar P, James EK, Reddy PM, Ladha JK. Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties. New Phytologist 2002; 154:131–145.

Boddey RM, Baldani VLD, Baldani JI, Döbereiner J. Effect of inoculation of Azospirillum spp. on the nitrogen assimilation of field grown wheat. Plant and Soil 1986; 95:109–121.

Taulé C, Mareque C, Barlocco C, Hackembruch F, Reis VM, Sicardi M et al. The contribution of nitrogen fixation to sugarcane (Saccharum officinarum L.), and the identification and characterization of part of the associated diazotrophic bacterial community. Plant and Soil 2012; 356:35–49.

Malik KA, Rakhshanda B, Mehnaz S, Rasul G, Mirza MS, Ali S. Association of nitrogen-fixing, plant-growth-promoting rhizobacteria (PGPR) with kallar grass and rice. Plant and Soil 1997; 194:37–48.

Hedin LO, Brookshire ENJ, Menge DNL, Barron AR. The nitrogen paradox in tropical forest ecosystems. Annual Review of Ecology, Evolution and Systematics 2002; 40:613–35.

Wurzburger N, Hedin LO. Taxonomic identity determines N2 fixation by canopy trees across lowland tropical forests. Ecology Letters 2016; 19:62–70. doi: 10.1111/ele.12543 PubMed DOI

Ritchie ME, Raina R. Effects of herbivores on nitrogen fixation by grass endophytes, legume symbionts and free-living soil surface bacteria in the Serengeti. Pedobiologia 2016; 59: 233–241.

Högberg P. Tansley Review No. 95,15N natural abundance in soil-plant systems. New Phytologist 1997; 137:179–203. PubMed

Shearer G, Kohl DH. N2-fixation in field settings: estimations based on natural 15N abundance. Australian Journal of Plant Physiology 1986; 13:699–756.

Evans RD. Physiological mechanisms influencing plant nitrogen isotope composition. TRENDS in Plant Science 2001; 6:121–126. PubMed

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