Nitrate storage and dissimilatory nitrate reduction by eukaryotic microbes

Frontiers in Microbiology

Volumn 6, Issue DEC, 2015, Pages

  Kamp, Anja ^a   Høgslund, Signe ^a   Risgaard Petersen, Nils ^a   Stief, Peter ^b  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Denitrification; Diatoms; DNRA; Foraminifers; Fungi; Gromiids; Nitrate respiration; Nitrogen cycle

Indexed keywords

AMMONIA; NITRATE; OXYGEN;

CILIATE; DENITRIFICATION; DIATOM; DINOFLAGELLATE; ECOPHYSIOLOGY; ENERGY CONSERVATION; ENVIRONMENTAL IMPACT; EUKARYOTE; EUKARYOTE EVOLUTION; FORAMINIFER; FUNGUS; GREEN ALGA; GROMIIDS; HABITAT; HAPTOPHYTA; LIFESTYLE; MARINE ENVIRONMENT; MICROBIAL METABOLISM; NITRATE METABOLISM; NITROGEN CYCLE; NONHUMAN; REVIEW;

EID: 84954242870     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01492     Document Type: Review

References (137)

1. Aleya, L., Hartmann, H. J., and Devaux, J. (1992). Evidence for the contribution of ciliates to denitrification in a eutrophic lake. Eur. J. Protistol. 28, 316-321. doi: 10.1016/S0932-4739(11)80238-5.
2. Allen, A. E., Vardi, A., and Bowler, C. (2006). An ecological and evolutionary context for integrated nitrogen metabolism and related signaling pathways in marine diatoms. Curr. Opin. Plant Biol. 9, 264-273. doi: 10.1016/j.pbi.2006.03.013.
3. Alve, E., and Bernhard, J. M. (1995). Vertical migratory response of benthic foraminifera to controlled oxygen concentrations in an experimental mesocosm. Mar. Ecol. Prog. Ser. 116, 137-151. doi: 10.3354/meps116137.
4. Anbar, A. D., and Knoll, A. H. (2002). Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137-1142. doi: 10.1126/science.1069651.
5. Armbrust, E. V. (2009). The life of diatoms in the world's oceans. Nature 459, 185-192. doi: 10.1038/nature08057.
6. Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martinez, D., Putnam, N. H., et al. (2004). The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79-86. doi: 10.1126/science.1101156.
7. Arnold, Z. M. (1972). Observations on the biology of the protozoan Gromia oviformis. Univ. Calif. Publ. Zool. 100, 1-168.
8. Bernhard, J. M., Casciotti, K. L., McIlvin, M. R., Beaudoin, D. J., Visscher, P. T., and Edgcomb, V. P. (2012b). Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration. J. Geophys. Res. 117, G03002. doi: 10.1029/2012JG001949.
9. Bernhard, J. M., Edgcomb, V. P., Casciotti, K. L., McIlvin, M. R., and Beaudoin, D. J. (2012a). Denitrification likely catalyzed by endobionts in an allogromiid foraminifer. ISME J 6, 951-960. doi: 10.1038/ismej.2011.171.
10. Bernhard, J. M., Kormas, K., Pachiadaki, M. G., Rocke, E., Beaudoin, D. J., Morrison, C., et al. (2014). Benthic protists and fungi of Mediterranean deep hypsersaline anoxic basin redoxcline sediments. Front. Microbiol. 5:605. doi: 10.3389/fmicb.2014.00605.
11. Bowler, C., Allen, A. E., Badger, J. H., Grimwood, J., Jabbari, K., Kuo, A., et al. (2008). The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239-244. doi: 10.1038/nature07410.
12. Brocks, J. J., Logan, G. A., Buick, R., and Summons, R. E. (1999). Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033-1036. doi: 10.1126/science.285.5430.1033.
13. Burki, F., Kudryavtsev, A., Matz, M. V., Aglyamova, G. V., Bulman, S., Fiers, M., et al. (2010). Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evol. Biol. 10:377. doi: 10.1186/1471-2148-10-377.
14. Canfield, D. E. (1998). A new model for Proterozoic ocean chemistry. Nature 396, 450-453. doi: 10.1038/24839.
15. Canfield, D. E., Glazer, A. N., and Falkowski, P. G. (2010). The evolution and future of earth's nitrogen cycle. Science 330, 192-196. doi: 10.1126/science.1186120.
16. Canfield, D. E., Poulton, S. W., Knoll, A. H., Narbonne, G. M., Ross, G., Goldberg, T., et al. (2008). Ferruginous conditions dominated later neoproterozoic deep-water chemistry. Science 321, 949-952. doi: 10.1126/science.1154499.
17. Chen, H. H., Mothapo, N. V., and Shi, W. (2014). The significant contribution of fungi to soil N2O production across diverse ecosystems. Appl. Soil Ecol. 73, 70-77. doi: 10.1016/j.apsoil.2013.08.011.
18. Consalvey, M., Paterson, D. M., and Underwood, G. J. C. (2004). The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Res. 19, 181-202. doi: 10.1080/0269249X.2004.9705870.
19. Coppens, J., Decostere, B., Van Hulle, S., Nopens, I., Vlaeminck, S. E., De Gelder, L., et al. (2014). Kinetic exploration of nitrate-accumulating microalgae for nutrient recovery. Appl. Microbiol. Biotechnol. 98, 8377-8387. doi: 10.1007/s00253-014-5854-9.
20. Crenshaw, C. L., Lauber, C., Sinsabaugh, R. L., and Stavely, L. K. (2008). Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry 87, 17-27. doi: 10.1007/s10533-007-9165-4.
21. da Silva, A. A., and Gooday, A. J. (2009). Large organic-walled Protista (Gromia) in the Arabian Sea: density, diversity, distribution and ecology. Deep Sea Res. II 56, 422-433. doi: 10.1016/j.dsr2.2008.12.027.
22. De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J. M., Thomine, S., Gambale, F., et al. (2006). The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442, 939-942. doi: 10.1038/nature05013.
23. Dortch, Q., Clayton, J. R. Jr., Thoresen, S. S., and Ahmed, S. I. (1984). Species differences in accumulation of nitrogen pools in phytoplankton. Mar. Biol. 81, 237-250. doi: 10.1007/BF00393218.
24. Edgcomb, V., Orsi, W., Taylor, G. T., Vdacny, P., Taylor, C., Suarez, P., et al. (2011). Accessing marine protists from the anoxic Cariaco Basin. ISME J. 5, 1237-1241. doi: 10.1038/ismej.2011.10.
25. Fennel, K., Follows, M., and Falkowski, P. G. (2005). The co-evolution of the nitrogen, carbon and oxygen cycles in the Proterozoic ocean. Amer. J. Sci. 305, 526-545. doi: 10.2475/ajs.305.6-8.526.
26. Fewson, C. A., and Nicholas, D. J. D. (1961). Utilization of nitrate by micro-organisms. Nature 190, 2-7. doi: 10.1038/190002a0.
27. Finlay, B. J. (1985). Nitrate respiration by Protozoa (Loxodes spp.) in the hypolimnetic nitrite maximum of a productive freshwater pond. Freshw. Biol. 15, 333-346. doi: 10.1111/j.1365-2427.1985.tb00205.x.
28. Finlay, B. J., Span, A. S. W., and Harman, J. M. P. (1983). Nitrate respiration in primitive eukaryotes. Nature 303, 333-336. doi: 10.1038/303333a0.
29. Fossing, H., Gallardo, V. A., Jørgensen, B. B., Hüttel, M., Nielsen, L. P., Schulz, H., et al. (1995). Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374, 713-715. doi: 10.1038/374713a0.
30. Foster, R. A., and Zehr, J. P. (2006). Characterization of diatom-cyanobacteria symbioses on the basis of nifH, hetR and 16S rRNA sequences. Environ. Microbiol. 8, 1913-1925. doi: 10.1111/j.1462-2920.2006.01068.x.
31. Frederiksen, M. S., and Glud, R. N. (2006). Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study. Limnol. Oceanogr. 51, 1072-1083. doi: 10.4319/lo.2006.51.2.1072.
32. García-Robledo, E., Corzo, A., Papaspyrou, S., Jiménez-Arias, J. L., and Villahermosa, D. (2010). Freeze-lysable inorganic nutrients in intertidal sediments: dependence on microphytobenthos abundance. Mar. Ecol. Prog. Ser. 403, 155-163. doi: 10.3354/meps08470.
33. Geslin, E., Heinz, P., Jorissen, F., and Hemleben, C. (2004). Migratory responses of deep-sea benthic foraminifera to variable oxygen conditions: laboratory investigations. Mar. Micropaleontol. 53, 227-243. doi: 10.1016/j.marmicro.2004.05.010.
34. Geslin, E., Risgaard-Petersen, N., Lombard, F., Metzger, E., Langlet, D., and Jorissen, F. (2011). Oxygen respiration rates of benthic foraminifera as measured with oxygen microsensors. J. Exp. Mar. Biol. Ecol. 396, 108-114. doi: 10.1016/j.jembe.2010.10.011.
35. Glock, N., Schönfeld, J., Eisenhauer, A., Hensen, C., Mallon, J., and Sommer, S. (2013). The role of benthic foraminifera in the benthic nitrogen cycle of the Peruvian oxygen minimum zone. Biogeoscience 10, 4767-4783. doi: 10.5194/bg-10-4767-2013.
36. Glud, R. N., Thamdrup, B., Stahl, H., Wenzhoefer, F., Glud, A., Nomaki, H., et al. (2009). Nitrogen cycling in a deep ocean margin sediment (Sagami Bay, Japan). Limnol. Oceanogr. 54, 723-734. doi: 10.4319/lo.2009.54.3.0723.
37. Gray, M. W. (2015). Mosaic nature of the mitochondrial proteome: implications for the origin and evolution of mitochondria. Proc. Natl. Acad. Sci. U.S.A. 112, 10133-10138. doi: 10.1073/pnas.1421379112.
38. Groffman, P. M., Altabet, M. A., Böhlke, J. K., Butterbach-Bahl, K., David, M. B., Firestone, M. K., et al. (2006). Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol. Appl. 16, 2091-2122. doi: 10.1890/1051-0761(2006)016[2091:MFMDDA]2.0.CO;2.
39. Groussin, M., Pawlowski, J., and Yang, Z. (2011). Bayesian relaxed clock estimation of divergence times in foraminifera. Mol. Phyl. Evol. 61, 157-166. doi: 10.1016/j.ympev.2011.06.008.
40. Härnström, K., Ellegaard, M., Andersen, T. J., and Godhe, A. (2011). Hundred years of genetic structure in a sediment revived diatom population. Proc. Natl. Acad. Sci. U.S.A. 108, 4252-4257. doi: 10.1073/pnas.1013528108.
41. Harold, F. M. (1986). The Vital Force: A Study of Bioenergetics. New York, NY: Freeman and Co.
42. Hedley, R. H., and Bertaud, W. S. (1962). Electron-microscopic observations of Gromia oviformis (Sarcodina). J. Protozool. 9, 79-87. doi: 10.1111/j.1550-7408.1962.tb02585.x.
43. Heisterkamp, I. M., Kamp, A., Schramm, A. T., de Beer, D., and Stief, P. (2012). Indirect control of the intracellular nitrate pool of intertidal sediment by the polychaete Hediste diversicolor. Mar. Ecol. Prog. Ser. 445, 181-192. doi: 10.3354/meps09464.
44. Høgslund, S. (2008). Nitrate Storage as an Adaption to Benthic Life. Ph.D. thesis, University of Aarhus, Aarhus.
45. Høgslund, S., Nielsen, J. L., and Nielsen, L. P. (2010). Distribution, ecology and molecular identification of Thioploca from Danish brackish water sediments. FEMS Microbiol. Ecol. 73, 110-120. doi: 10.1111/j.1574-6941.2010.00878.x.
46. Høgslund, S., Revsbech, N. P., Cedhagen, T., Nielsen, L. P., and Gallardo, V. A. (2008). Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile. J. Exp. Mar. Biol. Ecol. 359, 85-91. doi: 10.1016/j.jembe.2008.02.015.
47. Jepps, M. W. (1926). Contribution to the study of Gromia oviforinis Dujardin. Q. J. Microsc. Sci. 70, 701-719.
48. John, P., and Whatley, F. R. (1975). Paracoccus denitrificans and the evolutionary origin of the mitochondrion. Nature 254, 495-498. doi: 10.1038/254495a0.
49. Jørgensen, B. B., and Gallardo, V. A. (1999). Thioploca spp.: filamentous sulfur bacteria with nitrate vacuoles. FEMS Microbiol. Ecol. 28, 301-313. doi: 10.1016/S0168-6496(98)00122-6.
50. Kamp, A., de Beer, D., Nitsch, J. L., Lavik, G., and Stief, P. (2011). Diatoms respire nitrate to survive dark and anoxic conditions. Proc. Natl. Acad. Sci. U.S.A. 108, 5649-5654. doi: 10.1073/pnas.1015744108.
51. Kamp, A., Stief, P., Knappe, J., and de Beer, D. (2013). Response of the ubiquitous pelagic diatom Thalassiosira weissflogii to darkness and anoxia. PLoS ONE 8:e82605. doi: 10.1371/journal.pone.0082605.
52. Keeling, P. J., Burki, F., Wilcox, H. M., Allam, B., Allen, E. E., Amaral-Zettler, L. A., et al. (2014). The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 12:e1001889. doi: 10.1371/journal.pbio.1001889.
53. Kim, S. W., Fushinobu, S., Zhou, S., Wakagi, T., and Shoun, H. (2009). Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion? Appl. Environ. Microbiol. 75, 2652-2658. doi: 10.1128/AEM.02536-08.
54. Kim, S. W., Fushinobu, S., Zhou, S., Wakagi, T., and Shoun, H. (2010). The possible involvement of copper-containing nitrite reductase (NirK) and flavohemoglobin in denitrification by the fungus Cylindrocarpon tonkinense. Biosci. Biotechnol. Biochem. 74, 1403-1407. doi: 10.1271/bbb.100071.
55. Kingston, M. B. (1999). Wave effects on the vertical migration of two benthic microalgae: Hantzschia virgata var. intermedia and Euglena proxima. Estuaries 22, 81-91. doi: 10.2307/1352929.
56. Kizawa, H., Tomura, D., Oda, M., Fukamizu, A., Hoshino, T., Gotoh, O., et al. (1991). Nucleotide sequence of the unique nitrate/nitrite-inducible cytochrome P-450 cDNA from Fusarium oxysporum. J. Biol. Chem. 266, 10632-10637.
57. Klawonn, I., Bonaglia, S., Brüchert, V., and Ploug, H. (2015). Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates. ISME J. 9, 1456-1466. doi: 10.1038/ismej.2014.232.
58. Klionsky, D. J., Herman, P. K., and Emr, S. D. (1990). The fungal vacuole: composition, function, and biogenesis. Microbiol. Rev. 54, 266-292.
59. Kluyver, A. J., and Donker, H. J. L. (1926). Die Einheit in der Biochemie. Chem. Zelle Gewebe 13, 134-190.
60. Kobayashi, D. Y., and Crouch, J. A. (2009). Bacterial/fungal Interactions: from pathogens to mutualistic endosymbionts. Annu. Rev. Phytopathol. 47, 63-82. doi: 10.1146/annurev-phyto-080508-081729.
61. Kobayashi, M., Matsuo, Y., Takimoto, A., Suzuki, S., Maruo, F., and Shoun, H. (1996). Denitrification, a novel type of respiratory metabolism in fungal mitochondrion. J. Biol. Chem. 271, 16263-16267. doi: 10.1074/jbc.271.27.16263.
62. Koho, K. A., Piña-Ochoa, E., Geslin, E., and Risgaard-Petersen, N. (2011). Vertical migration, nitrate uptake and denitrification: survival mechanisms of foraminifers (Globobulimina turgida) under low oxygen conditions. FEMS Microbiol. Ecol. 75, 273-283. doi: 10.1111/j.1574-6941.2010.01010.x.
63. Kraft, B., Strous, M., and Tegetmeyer, H. E. (2011). Microbial nitrate respiration-Genes, enzymes and environmental distribution. J. Biotechnol. 155, 104-117. doi: 10.1016/j.jbiotec.2010.12.025.
64. Kristensen, E., Jensen, M. H., and Aller, R. C. (1991). Direct measurement of dissolved inorganic nitrogen exchange and denitrification in individual polychaete (Nereis virens) burrows. J. Mar. Res. 49, 355-377. doi: 10.1357/002224091784995855.
65. Larsen, M., Thamdrup, B., Shimmield, T., and Glud, R. N. (2013). Benthic mineralization and solute exchange on a Celtic Sea sand-bank (Jones Bank). Prog. Oceanogr. 117, 64-75. doi: 10.1016/j.pocean.2013.06.010.
66. Laughlin, R., and Stevens, R. (2002). Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Sci. Soc. Am. J. 66, 1540-1548. doi: 10.2136/sssaj2002.1540.
67. Lomas, M., and Glibert, P. (2000). Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J. Phycol. 36, 903-913. doi: 10.1046/j.1529-8817.2000.99029.x.
68. Lomas, M. W., and Glibert, P. M. (1999). Temperature regulation of nitrate uptake: a novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnol. Oceanogr. 44, 556-572. doi: 10.4319/lo.1999.44.3.0556.
69. Lomstein, E., Jensen, M. H., and Sørensen, J. (1990). Intracellular NH4+ and NO3-pools associated with deposited phytoplankton in a marine sediment (Aarhus Bight, Denmark). Mar. Ecol. Prog. Ser. 61, 97-105. doi: 10.3354/meps061097.
70. Long, A., Song, B., Fridey, K., and Silva, A. (2015). Detection and diversity of copper containing nitrite reductase genes (nirK) in prokaryotic and fungal communities of agricultural soils. FEMS Microbiol. Ecol. 91, 1-9. doi: 10.1093/femsec/fiu004.
71. Lücking, R., Huhndorf, S., Pfister, D. H., Plata, E. R., and Lumbsch, H. T. (2009). Fungi evolved right on track. Mycologia 101, 810-822. doi: 10.3852/09-016.
72. Lyons, T. W., Reinhard, C. T., and Planavsky, N. J. (2014). The rise of oxygen in Earth's early ocean and atmosphere. Nature 506, 307-315. doi: 10.1038/nature13068.
73. Maeda, K., Spor, A., Edel-Hermann, V., Heraud, C., Breuil, M. C., Bizouard, F., et al. (2015). N2O production, a widespread trait in fungi. Sci. Rep. 5, 9697. doi: 10.1038/srep09697.
74. Marchant, H. K., Lavik, G., Holtappels, M., and Kuypers, M. M. (2014). The fate of nitrate in intertidal permeable sediments. PLoS ONE 9:e104517. doi: 10.1371/journal.pone.0104517.
75. Martin, W., Rotte, C., Hoffmeister, M., Theissen, U., Gelius-Dietrich, G., Ahr, S., et al. (2003). Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55, 193-204. doi: 10.1080/1521654031000141231.
76. Martinoia, E., Heck, U., and Wiemken, A. (1981). Vacuoles as storage compartments for nitrate in barley leaves. Nature 289, 292-294. doi: 10.1038/289292a0.
77. Matz, M. V., Frank, T. M., Marshall, N. J., Widder, E. A., and Johnsen, S. (2008). Giant deep-sea protist produces bilaterian-like traces. Curr. Biol. 18, 1849-1854. doi: 10.1016/j.cub.2008.10.028.
78. McHatton, S. C., Barry, J. P., Jannasch, H. W., and Nelson, D. C. (1996). High nitrate concentrations in vacuolate, autotrophic marine Beggiatoa spp. Appl. Environ. Microbiol. 62, 954-958.
79. Medlin, L. K. (2011). "A review of the evolution of the diatoms from the origin of the lineage to their populations," in The Diatom World, Cellular Origin, Life in Extreme Habitats and Astrobiology, Vol. 19, eds J. Seckbach and J. P. Kociolek (Dordrecht; Heidelberg; London; New York, NY: Springer), 93-118. doi: 10.1007/978-94-007-1327-7_4.
80. Mentel, M., and Martin, W. (2008). Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 2717-2729. doi: 10.1098/rstb.2008.0031.
81. Mothapo, N., Chen, H. H., Cubeta, M. A., Grossman, J. M., Fuller, F., and Shi, W. (2015). Phylogenetic, taxonomic and functional diversity of fungal denitrifiers and associated N2O production efficacy. Soil Biol. Biochem. 83, 160-175. doi: 10.1016/j.soilbio.2015.02.001.
82. Mothapo, N. V., Chena, H., Cubetab, M. A., and Shi, W. (2013). Nitrous oxide producing activity of diverse fungi from distinct agroecosystems. Soil Biol. Biochem. 66, 94-101. doi: 10.1016/j.soilbio.2013.07.004.
83. Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., et al. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444-495. doi: 10.1128/MMBR.05024-11.
84. Mußmann, M., Hu, F. Z., Richter, M., de Beer, D., Preisler, A., Jørgensen, B. B., et al. (2007). Insights into the genome of large sulfur bacteria revealed by analysis of single filaments. PLoS Biol. 5:e230. doi: 10.1371/journal.pbio.0050230.
85. Navarro, F. J., Machín, F., Martín, Y., and Siverio, J. M. (2006). Down-regulation of eukaryotic nitrate transporter by nitrogen-dependent ubiquitinylation. J. Biol. Chem. 281, 13268-13274. doi: 10.1074/jbc.M601253200.
86. Needoba, J. A., and Harrison, P. J. (2004). Influence of low light and a light: dark cycle on NO3-uptake, intracellular NO3-, and nitrogen isotope fractionation by marine phytoplankton. J. Phycol. 40, 505-516. doi: 10.1111/j.1529-8817.2004.03171.x.
87. Nielsen, L. P. (1992). Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiol. Lett. 86, 357-362. doi: 10.1111/j.1574-6968.1992.tb04828.x.
88. Nomaki, H., Chikaraishi, Y., Tsuchiya, M., Toyofuku, T., Ohkouchi, N., Uematsu, K., et al. (2014). Nitrate uptake by foraminifera and use in conjunction with endobionts under anoxic conditions. Limnol. Oceanogr. 59, 879-1888. doi: 10.4319/lo.2014.59.6.1879.
89. Nomaki, H., Chikaraishi, Y., Tsuchiya, M., Toyofuku, T., Suga, H., Sasaki, Y., et al. (2015). Variation in the nitrogen isotopic composition of amino acids in benthic foraminifera: implications for their adaptation to oxygen-depleted environments. Limnol. Oceanogr. 60, 1906-1916. doi: 10.1002/lno.10140.
90. Papaspyrou, S., Smith, C. J., Dong, L. F., Whitby, C., Dumbrell, A. J., and Nedwell, D. B. (2014). Nitrate reduction functional genes and nitrate reduction potentials persist in deeper estuarine sediments. Why? PLoS ONE 9:e94111. doi: 10.1371/journal.pone.0094111.
91. Parris, D. J., Ganesh, S., Edgcomb, V. P., DeLong, E. F., and Stewart, F. J. (2014). Microbial eukaryote diversity in the marine oxygen minimum zone off northern Chile. Front. Microbiol. 5:543. doi: 10.3389/fmicb.2014.00543.
92. Pawlowski, J., Holzmann, M., Berney, C., Fahrni, J., Gooday, A. J., Cedhagen, T., et al. (2003). The evolution of early Foraminifera. Proc. Natl. Acad. Sci. U.S.A. 100, 11494-11498. doi: 10.1073/pnas.2035132100.
93. Piña-Ochoa, E., Høgslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P., Nielsen, L. P., et al. (2010a). Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida. Proc. Natl. Acad. Sci. U.S.A. 107, 1148-1153. doi: 10.1073/pnas.0908440107.
94. Piña-Ochoa, E., Koho, K. A., Geslin, E., and Risgaard-Petersen, N. (2010b). Survival and life strategy of the foraminiferan Globobulimina turgida through nitrate storage and denitrification. Mar. Ecol. Prog. Ser. 417, 39-49. doi: 10.3354/meps08805.
95. Ploug, H., Kühl, M., Buchholz-Cleven, B., and Jørgensen, B. B. (1997). Anoxic aggregates-an ephemeral phenomenon in the pelagic environment? Aquat. Microb. Ecol. 13, 285-294. doi: 10.3354/ame013285.
96. Prendergast-Miller, M. T., Baggs, E. M., and Johnson, D. (2011). Nitrous oxide production by the ectomycorrhizal fungi Paxillus involutus and Tylospora fibrillosa. FEMS Microbiol. Lett. 316, 31-35. doi: 10.1111/j.1574-6968.2010.02187.x.
97. Prieto, M., and Wedin, M. (2013). Dating the diversification of the major lineages of Ascomycota (Fungi). PloS ONE 8:e65576. doi: 10.1371/journal.pone.0065576.
98. Prihoda, J., Tanaka, A., de Paula, W. B. M., Allen, J. F., Tirichine, L., and Bowler, C. (2012). Chloroplast-mitochondria cross-talk in diatoms. J. Exp. Bot. 63, 1543-1557. doi: 10.1093/jxb/err441.
99. Prokopenko, M. G., Sigman, D. M., Berelson, W. M., Hammond, D. E., Barnett, B., Chong, L., et al. (2011). Denitrification in anoxic sediments supported by biological nitrate transport. Geochim. Cosmochim. Acta 75, 7180-7199. doi: 10.1016/j.gca.2011.09.023.
100. Raimbault, P., and Mingazzini, M. (1987). Diurnal variations of intracellular nitrate storage by marine diatoms: effects of nutritional state. J. Exp. Mar. Biol. Ecol. 112, 217-232. doi: 10.1016/0022-0981(87)90070-0.
101. Revsbech, N. P., Sorensen, J., Blackburn, T. H., and Lomholt, J. P. (1980). Distribution of oxygen in marine sediments measured with microelectrodes. Limnol. Oceanogr. 25, 403-411. doi: 10.4319/lo.1980.25.3.0403.
102. Risgaard-Petersen, N., and Jensen, K. (1997). Nitrification and denitrification in the rhizosphere of the aquatic macrophyte Lobelia dortmanna L. Limnol. Oceanogr. 42, 529-537. doi: 10.4319/lo.1997.42.3.0529.
103. Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C., Jetten, M. S. M., Op den Camp, H. J. M., et al. (2006). Evidence for complete denitrification in a benthic foraminifer. Nature 443, 93-96. doi: 10.1038/nature05070.
104. Rothe, N., Gooday, A. J., Cedhagen, T., and Hughes, J. A. (2011). Biodiversity and distribution of the genus Gromia (Protista, Rhizaria) in the deep Weddell Sea (Southern Ocean). Polar Biol. 34, 69-81. doi: 10.1007/s00300-010-0859-z.
105. Satkoski, A. M., Beukes, N. J., Li, W., Beard, B. L., and Johnson, C. M. (2015). A redox-stratified ocean 3.2 billion years ago. Earth Planet Sci. Lett. 430, 43-53. doi: 10.1016/j.epsl.2015.08.007.
106. Sayama, M. (2001). Presence of nitrate-accumulating sulfur bacteria and their influence on nitrogen cycling in a shallow coastal marine sediment. Appl. Environ. Microbiol. 67, 3481-3487. doi: 10.1128/AEM.67.8.3481-3487.2001.
107. Schulz, H. N., Brinkhoff, T., Ferdelman, T. G., Mariné, M. H., Teske, A., and Jørgensen, B. B. (1999). Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 284, 493-495. doi: 10.1126/science.284.5413.493.
108. Shoun, H., Fushinobu, S., Jiang, L., Kim, S.-W., and Wakagi, T. (2012). Fungal denitrification and nitric oxide reductase cytochrome P450nor. Philos. Trans. R. Soc. B 367, 1186-1194. doi: 10.1098/rstb.2011.0335.
109. Shoun, H., and Tanimoto, T. (1991). Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in the respiratory nitrite reduction. J. Biol. Chem. 266, 11078-11082.
110. Sierra, R., Matz, M. V., Aglyamova, G., Pillet, L., Decelle, J., Not, F., et al. (2013). Deep relationships of Rhizaria revealed by phylogenomics: a farewell to Haeckel's Radiolaria. Mol. Phylogenet. Evol. 67, 53-59. doi: 10.1016/j.ympev.2012.12.011.
111. Sims, P. A., Mann, D. G., and Medlin, L. K. (2006). Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45, 361-402. doi: 10.2216/05-22.1.
112. Steward, C. C., Nold, S. C., Ringelberg, D. B., White, D. C., and Lovell, C. R. (1996). Microbial biomass and community structures in the burrows of bromophenol producing and non-producing marine worms and surrounding sediments. Mar. Ecol. Prog. Ser. 133, 149-165. doi: 10.3354/meps133149.
113. Stief, P., and de Beer, D. (2006). Probing the microenvironment of freshwater sediment macrofauna: implications of deposit-feeding and bioirrigation for nitrogen cycling. Limnol. Oceanogr. 51, 2538-2548. doi: 10.4319/lo.2006.51.6.2538.
114. Stief, P., Fuchs-Ocklenburg, S., Kamp, A., Manohar, C. S., Houbraken, J., Boekhout, T., et al. (2014). Dissimilatory nitrate reduction by Aspergillus terreus isolated from the seasonal oxygen minimum zone in the Arabian Sea. BMC Microbiol. 14:35. doi: 10.1186/1471-2180-14-35.
115. Stief, P., Kamp, A., and de Beer, D. (2013). Role of diatoms in the spatial-temporal distribution of intracellular nitrate in intertidal sediment. PLoS ONE 8:e73257. doi: 10.1371/journal.pone.0073257.
116. Stoeck, T., Behnke, A., Christen, R., Amaral-Zettler, L., Rodriguez-Mora, M. J., Chistoserdov, A., et al. (2009). Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities. BMC Biol. 7:72. doi: 10.1186/1741-7007-7-72.
117. Strohm, T. O., Griffin, B., Zumft, W. G., and Schink, B. (2007). Growth yields in bacterial denitrification and nitrate ammonification. Appl. Environ. Microbiol. 73, 1420-1424. doi: 10.1128/AEM.02508-06.
118. Sweerts, J.-P. R. A., and de Beer, D. (1989). Microelectrode measurements of nitrate gradients in the littoral and profundal sediments of a meso-eutrophic lake (Lake Vechten, The Netherlands). Appl. Environ. Microbiol. 55, 754-757.
119. Takasaki, K., Shoun, H., Yamaguchi, M., Takeo, K., Nakamura, A., Hoshino, T., et al. (2004). Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol-Role of acetyl CoA synthetase in anaerobic ATP synthesis. J. Biol. Chem. 279, 12414-12420. doi: 10.1074/jbc.M313761200.
120. Takaya, N. (2009). Response to hypoxia, reduction of electron acceptors, and subsequent survival by filamentous fungi. Biosci. Biotechnol. Biochem. 73, 1-8. doi: 10.1271/bbb.80487.
121. Takaya, N., Suzuki, S., Kuwazaki, S., Shoun, H., Maruo, F., Yamaguchi, M., et al. (1999). Cytochrome p450nor, a novel class of mitochondrial cytochrome P450 involved in nitrate respiration in the fungus Fusarium oxysporum. Arch. Biochem. Biophys. 372, 340-346. doi: 10.1006/abbi.1999.1499.
122. Tantanasarit, C., Englande, A., and Babel, S. (2013). Nitrogen, phosphorus and silicon uptake kinetics by marine diatom Chaetoceros calcitrans under high nutrient concentrations. J. Exp. Mar. Biol. Ecol. 446, 67-75. doi: 10.1016/j.jembe.2013.05.004.
123. Thamdrup, B. (2012). New Pathways and processes in the global nitrogen cycle. Annu. Rev. Ecol. Evol. Syst. 43, 407-428. doi: 10.1146/annurev-ecolsys-102710-145048.
124. Thornton, D. C. O. (2002). Diatom aggregation in the sea: mechanisms and ecological implications. Eur. J. Phycol. 37, 149-161. doi: 10.1017/S0967026202003657.
125. Tsuruta, S., Takaya, N., Zhang, L., Shoun, H., Kimura, K., Hamamoto, M., et al. (1998). Denitrification by yeasts and occurrence of cytochrome P450nor in Trichosporon cutaneum. FEMS Microbiol. Lett. 168, 105-110. doi: 10.1111/j.1574-6968.1998.tb13262.x.
126. Unkles, S. E., Wang, R. C., Wang, Y., Glass, A. D. M., Crawford, N. M., and Kinghorn, J. R. (2004). Nitrate reductase activity is required for nitrate uptake into fungal but not plant cells. J. Biol. Chem. 279, 28182-28186. doi: 10.1074/jbc.M403974200.
127. Usuda, K., Toritsuka, N., Matsuo, Y., Kim, D. H., and Shoun, H. (1995). Denitrification by the fungus Cylindrocarpon tonkinense: anaerobic cell growth and two isozyme forms of cytochrome P-450nor. Appl. Environ. Microbiol. 61, 883-889.
128. van der Giezen, M. (2011). Mitochondria and the rise of eukaryotes. Bioscience 61, 594-601. doi: 10.1525/bio.2011.61.8.5.
129. Villareal, T. A., Altabet, M. A., and Culverrymsza, K. (1993). Nitrogen transport by vertically migrating diatom mats in the North Pacific Ocean. Nature 363, 709-712. doi: 10.1038/363709a0.
130. Villareal, T. A., Joseph, L., Brzezinski, M. A., Shipe, R. F., Lipschultz, F., and Altabet, M. A. (1999). Biological and chemical characteristics of the giant diatom Ethmodiscus (Bacillariophyceae) in the central north pacific gyre. J. Phycol. 35, 896-902. doi: 10.1046/j.1529-8817.1999.3550896.x.
131. Wei, W., Isobe, K., Shiratori, Y., Nishizawa, T., Ohte, N., Ise, Y., et al. (2015). Development of PCR primers targeting fungal nirK to study fungal denitrification in the environment. Soil Biol. Biochem. 81, 282-286. doi: 10.1016/j.soilbio.2014.11.026.
132. Wenzhöfer, F., and Glud, R. N. (2004). Small-scale spatial and temporal variability in coastal benthic O2 dynamics: effects of fauna activity. Limnol. Oceanogr. 49, 1471-1481. doi: 10.4319/lo.2004.49.5.1471.
133. Williams, K. P., Sobral, B. W., and Dickerman, A. W. (2007). A robust species tree for the Alphaproteobacteria. J. Bacteriol. 189, 4578-4586. doi: 10.1128/JB.00269-07.
134. Worden, A. Z., Follows, M. J., Giovannoni, S. J., Wilken, S., Zimmerman, A. E., and Keeling, P. J. (2015). Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347, 735. doi: 10.1126/science.1257594.
135. Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J., and Woese, C. R. (1985). Mitochondrial origins. Proc. Natl. Acad. Sci. U.S.A. 82, 4443-4447. doi: 10.1073/pnas.82.13.4443.
136. Zhou, Z., Takaya, N., Nakamura, A., Yamaguchi, M., Takeo, K., and Shoun, H. (2002). Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. J. Biol. Chem. 277, 1892-1896. doi: 10.1074/jbc.M109096200.
137. Zumft, W. G. (1997). Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533-616.