Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A

  • An Erratum to this article was published on 23 January 2017

Abstract

Nitrogen fixation — the reduction of dinitrogen (N2) gas to biologically available nitrogen (N) — is an important source of N for terrestrial and aquatic ecosystems. In terrestrial environments, N2-fixing symbioses involve multicellular plants, but in the marine environment these symbioses occur with unicellular planktonic algae. An unusual symbiosis between an uncultivated unicellular cyanobacterium (UCYN-A) and a haptophyte picoplankton alga was recently discovered in oligotrophic oceans. UCYN-A has a highly reduced genome, and exchanges fixed N for fixed carbon with its host. This symbiosis bears some resemblance to symbioses found in freshwater ecosystems. UCYN-A shares many core genes with the ‘spheroid bodies’ of Epithemia turgida and the endosymbionts of the amoeba Paulinella chromatophora. UCYN-A is widely distributed, and has diversified into a number of sublineages that could be ecotypes. Many questions remain regarding the physical and genetic mechanisms of the association, but UCYN-A is an intriguing model for contemplating the evolution of N2-fixing organelles.

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Figure 1
Figure 2: Phylogenetic trees showing the evolutionary relationship between UCYN-A and other cyanobacteria, as well as the microdiversity of UCYN-A and known UCYN-A hosts.
Figure 3: Methods used to discover the UCYN-A unicellular symbiosis.
Figure 4: Visualizations of UCYN-A from key observations between 2012–2016 using a variety of techniques.
Figure 5: Protein comparisons across genomes of UCYN-A1, the Paulinella chromatophore and the E. turgida spheroid body.
Figure 6: Schematic depictions of plastid evolution and cellular structures in the Paulinella and E. turgida symbiotic associations, and the potential symbiotic interactions in UCYN-A.

References

  1. 1

    Fowler, D. et al. The global nitrogen cycle in the twenty-first century. Phil. Trans. R. Soc. B 368, 20130164 (2013).

    Google Scholar 

  2. 2

    Raymond, J., Siefert, J. L., Staples, C. R. & Blankenship, R. E. The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541–554 (2004).

    CAS  Google Scholar 

  3. 3

    Kneip, C., Lockhart, P., Voss, C. & Maier, U. G. Nitrogen fixation in eukaryotes — new models for symbiosis. BMC Evol. Biol. 7, 55 (2007).

  4. 4

    Geurts, R., Xiao, T. T. & Reinhold-Hurek, B. What does it take to evolve a nitrogen-fixing endosymbiosis?. Trends Plant Sci. 21, 199–208 (2016).

    CAS  PubMed  Google Scholar 

  5. 5

    Vitousek, P. M. & Howarth R. W. Nitrogen limitation on land and in the sea: how can it occur?. Biogeochemistry 13, 87–115 (1991).

    Google Scholar 

  6. 6

    Redfield, A. C. The biological control of chemical factors in the environment. Am. Sci. 46, 205–222 (1958).

    CAS  Google Scholar 

  7. 7

    Ryther, J. & Dunstan, W. Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171, 1008–1013 (1971).

    CAS  PubMed  Google Scholar 

  8. 8

    Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem. Cy. 11, 235–266 (1997).

    CAS  Google Scholar 

  9. 9

    Codispoti, L. A. An oceanic fixed nitrogen sink exceeding 400 Tg N a−1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4, 233–253 (2007).

    CAS  Google Scholar 

  10. 10

    Capone, D., Zehr, J., Paerl, H. & Bergman, B. Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221–1229 (1997).

    CAS  Google Scholar 

  11. 11

    Mague, T. H., Mague, F. C. & Holm-Hansen, O. Physiology and chemical composition of nitrogen fixing phytoplankton in the central North Pacific Ocean. Mar. Biol. 41, 213–227 (1977).

    CAS  Google Scholar 

  12. 12

    Villareal, T. A. Nitrogen-fixation by the cyanobacterial symbiont of the diatom genus Hemiaulus. Mar. Ecol. Prog. Ser. 76, 201–204 (1991).

    CAS  Google Scholar 

  13. 13

    Villareal, T. A. in Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (eds Carpenter, E. J., Capone, D. G. & Rueter, J. G. ) 163–175 (Kluwer Academic, 1992).

    Google Scholar 

  14. 14

    Villareal, T. A. Widespread occurrence of the Hemiaulus-cyanobacterial symbiosis in the southwest North Atlantic Ocean. Bull. Mar. Sci. 54, 1–7 (1994).

    Google Scholar 

  15. 15

    Foster, R. A., Carpenter, E. J. & Bergman, B. Unicellular cyanobionts in open ocean dinoflagellates, radiolarians, and tintinnids: ultrastructural characterization and immuno-localization of phycoerythrin and nitrogenase. J. Phycol. 42, 453–463 (2006).

    CAS  Google Scholar 

  16. 16

    Zehr, J. & McReynolds, L. Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl. Environ. Microbiol. 55, 2522–2526 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Paerl, H. W., Prufert, L. E. & Ambrose, W. W. Contemporaneous N2 fixation and oxygenic photosynthesis in the nonheterocystous mat-forming cyanobacterium Lyngbya aestuarii. Appl. Environ. Microbiol. 57, 3086–3092 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

    Zehr, J., Mellon, M. & Zani, S. New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl. Environ. Microbiol. 64, 3444–3450 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19

    Zehr, J. et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635–638 (2001).

    CAS  PubMed  Google Scholar 

  20. 20

    Karl, D. M., Church, M. J., Dore, J. E., Letelier, R. M. & Mahaffey, C. Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc. Natl Acad. Sci. USA 109, 1842–1849 (2012).

    CAS  PubMed  Google Scholar 

  21. 21

    Dore, J. E., Brum, J. R., Tupas, L. M. & Karl, D. M. Seasonal and interannual variability in sources of nitrogen supporting export in the oligotrophic subtropical North Pacific Ocean. Limnol. Oceanogr. 47, 1595–1607 (2002).

    CAS  Google Scholar 

  22. 22

    Montoya, J. P. et al. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430, 1027–1031 (2004).

    CAS  PubMed  Google Scholar 

  23. 23

    Grabowski, M. N. W., Church, M. J. & Karl, D. M. Nitrogen fixation rates and controls at Stn ALOHA. Aquat. Microb. Ecol. 52, 175–183 (2008).

    Google Scholar 

  24. 24

    Falcón, L. I., Cipriano, F., Chistoserdov, A. Y. & Carpenter, E. J. Diversity of diazotrophic unicellular cyanobacteria in the tropical North Atlantic Ocean. Appl. Environ. Microbiol. 68, 5760–5764 (2002).

    PubMed  PubMed Central  Google Scholar 

  25. 25

    Mazard, S. L., Fuller, N. J., Orcutt, K. M., Bridle, O. & Scanlan, D. J. PCR analysis of the distribution of unicellular cyanobacterial diazotrophs in the Arabian Sea. Appl. Environ. Microbiol. 70, 7355–7364 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Church, M. J., Björkman, K. M., Karl, D. M., Saito, M. A. & Zehr, J. P. Regional distributions of nitrogen-fixing bacteria in the Pacific Ocean. Limnol. Oceanogr. 53, 63–77 (2008).

    CAS  Google Scholar 

  27. 27

    Langlois, R. J., Hummer, D. & LaRoche, J. Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Appl. Environ. Microbiol. 74, 1922–1931 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28

    Moisander, P. H. et al. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327, 1512–1514 (2010).

    CAS  Google Scholar 

  29. 29

    Halm, H. et al. Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J. 6, 1238–1249 (2012).

    CAS  PubMed  Google Scholar 

  30. 30

    Agawin, N. S. R. et al. Dominance of unicellular cyanobacteria in the diazotrophic community in the Atlantic Ocean. Limnol. Oceanogr. 59, 623–637 (2014).

    CAS  Google Scholar 

  31. 31

    Bentzon-Tilia, M. et al. Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J. 9, 273–285 (2015).

    CAS  PubMed  Google Scholar 

  32. 32

    Messer, L. F., Doubell, M., Jeffries, T. C., Brown, M. V. & Seymour, J. R. Prokaryotic and diazotrophic population dynamics within a large oligotrophic inverse estuary. Aquat. Microb. Ecol. 74, 1–15 (2015).

    Google Scholar 

  33. 33

    Shiozaki, T., Nagata, T., Ijichi, M. & Furuya, K. Nitrogen fixation and the diazotroph community in the temperate coastal region of the northwestern North Pacific. Biogeosciences 12, 4751–4764 (2015).

    Google Scholar 

  34. 34

    Luo, Y. W. et al. Database of diazotrophs in global ocean: abundance, biomass and nitrogen fixation rates. Earth Syst. Sci. Data 4, 47–73 (2012).

    Google Scholar 

  35. 35

    Farnelid, H., Turk-Kubo, K., Muñoz-Marín, M. d. C. & Zehr, J. P. New insights into the ecology of the globally significant uncultured nitrogen-fixing symbiont UCYN-A. Aquat. Microb. Ecol. 77, 125–138 (2016).

    Google Scholar 

  36. 36

    Biegala, I. C. & Raimbault, P. High abundance of diazotrophic picocyanobacteria ( <3 μm) in a Southwest Pacific coral lagoon. Aquat. Microb. Ecol. 51, 45–53 (2008).

    Google Scholar 

  37. 37

    Bonnet, S., Biegala, I. C., Dutrieux, P., Slemons, L. O. & Capone, D. G. Nitrogen fixation in the western equatorial Pacific: rates, diazotrophic cyanobacterial size class distribution, and biogeochemical significance. Glob. Biogeochem. Cycles 23, 3GB012 (2009).

    Google Scholar 

  38. 38

    Le Moal, M. & Biegala, I. C. Diazotrophic unicellular cyanobacteria in the northwestern Mediterranean Sea: a seasonal cycle. Limnol. Oceanogr. 54, 845–855 (2009).

    CAS  Google Scholar 

  39. 39

    Krupke, A. et al. In situ identification and N2 and C fixation rates of uncultivated cyanobacteria populations. Syst. Appl. Microbiol. 36, 259–271 (2013).

    CAS  PubMed  Google Scholar 

  40. 40

    Thompson, A. W. et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337, 1546–1550 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    Krupke, A. et al. Distribution of a consortium between unicellular algae and the N2 fixing cyanobacterium UCYN-A in the North Atlantic Ocean. Environ. Microbiol. 16, 3153–3167 (2014).

    CAS  PubMed  Google Scholar 

  42. 42

    Cabello, A. M. et al. Global distribution and vertical patterns of a prymnesiophyte-cyanobacteria obligate symbiosis. ISME J. 10, 693–706 (2016).

    PubMed  Google Scholar 

  43. 43

    Cornejo-Castillo, F. M. et al. Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton. Nat. Commun. 7, 11071 (2016).

  44. 44

    Fay, P. Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol. Mol. Biol. Rev. 56, 340–373 (1992).

    CAS  Google Scholar 

  45. 45

    Berman-Frank, I., Lundgren, P. & Falkowski, P. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res. Microbiol. 154, 157–164 (2003).

    CAS  PubMed  Google Scholar 

  46. 46

    Church, M. J., Short, C. M., Jenkins, B. D., Karl, D. M. & Zehr, J. P. Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl. Environ. Microbiol. 71, 5362–5370 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47

    Zehr, J. P. et al. Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110–1112 (2008).

    CAS  Google Scholar 

  48. 48

    Tripp, H. J. et al. Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464, 90–94 (2010).

    CAS  Google Scholar 

  49. 49

    Shi, X. L., Marie, D., Jardillier, L., Scanlan, D. J. & Vaulot, D. Groups without cultured representatives dominate eukaryotic picophytoplankton in the oligotrophic South East Pacific Ocean. PLoS ONE 4, e7657 (2009).

  50. 50

    Krupke, A. et al. The effect of nutrients on carbon and nitrogen fixation by the UCYN-A–haptophyte symbiosis. ISME J. 7, 1635–1647 (2015).

    Google Scholar 

  51. 51

    Needham, D. M. & Fuhrman, J. A. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat. Microbiol. 1, 16005 (2016).

  52. 52

    Hagino, K., Onuma, R., Kawachi, M. & Horiguchi, T. Discovery of an endosymbiotic nitrogen-fixing cyanobacterium UCYN-A in Braarudosphaera bigelowii (Prymnesiophyceae). PLoS ONE 8, e81749 (2013).

    PubMed  PubMed Central  Google Scholar 

  53. 53

    Thompson, A. et al. Genetic diversity of the unicellular nitrogen-fixing cyanobacteria UCYN-A and its prymnesiophyte host. Environ. Microbiol. 16, 3238–3249 (2014).

    CAS  PubMed  Google Scholar 

  54. 54

    Bombar, D., Heller, P., Sanchez-Baracaldo, P., Carter, B. J. & Zehr, J. P. Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria. ISME J. 8, 2530–2542 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55

    Zehr, J. How single cells work together: are single-celled symbioses organelle evolution in action?. Science 349, 1163–1164 (2015).

    CAS  PubMed  Google Scholar 

  56. 56

    Martínez-Pérez, C. et al. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat. Microbiol. 1, 16163 (2016).

  57. 57

    Carpenter, E. J. & Janson, S. Intracellular cyanobacterial symbionts in the marine diatom Climacodium frauenfeldianum (Bacillariophyceae). J. Phycol. 36, 540–544 (2000).

    PubMed  Google Scholar 

  58. 58

    Bench, S. R., Heller, P., Frank, I. & Arciniega, M. Whole genome comparison of six Crocosphaera watsonii strains with differing phenotypes. J. Phycol. 49, 786–801 (2013).

    PubMed  PubMed Central  Google Scholar 

  59. 59

    Ran, L. et al. Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. PLoS ONE 5, e11486 (2010).

    PubMed  PubMed Central  Google Scholar 

  60. 60

    Villareal, T. A. Evaluation of nitrogen fixation in the diatom genus Rhizosolenia Ehr. in the absence of its cyanobacterial symbiont Richelia intracellularis Schmidt. J. Plankton Res. 9, 965–971 (1987).

    Google Scholar 

  61. 61

    Villareal, T. A. Laboratory culture and preliminary characterization of the nitrogen-fixing Rhizosolenia-Richelia symbiosis. Mar. Ecol. 11, 117–132 (1990).

    CAS  Google Scholar 

  62. 62

    Nakayama, T. et al. Spheroid bodies in rhopalodiacean diatoms were derived from a single endosymbiotic cyanobacterium. J. Plant Res. 124, 93–97 (2011).

    PubMed  Google Scholar 

  63. 63

    Nakayama, T. et al. Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle. Proc. Natl Acad. Sci. USA 111, 11407–11412 (2014).

    CAS  PubMed  Google Scholar 

  64. 64

    Trapp, E. M., Adler, S. & Zauner, S. Rhopalodia gibba and its endosymbionts as a model for early steps in a cyanobacterial primary endosymbiosis. Endocytobiosis Cell Res. 23, 21–24 (2012).

    Google Scholar 

  65. 65

    Prechtl, J., Kneip, C., Lockhart, P., Wenderoth, K. & Maier, U. G. Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol. Biol. Evol. 21, 1477–1481 (2004).

    CAS  PubMed  Google Scholar 

  66. 66

    Hagino, K. et al. Extracellular calcification of Braarudosphaera bigelowii deduced from electron microscopic observations of cell surface structure and elemental composition of pentaliths. Mar. Micropaleontol. 125, 85–94 (2016).

    Google Scholar 

  67. 67

    Kolber, Z. S. et al. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292, 2492–2495 (2001).

    CAS  PubMed  Google Scholar 

  68. 68

    Frías, J. E., Flores, E. & Herrero, A. Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC7120. Mol. Microbiol. 14, 823–832 (1994).

    PubMed  Google Scholar 

  69. 69

    Herrero, A., Muro-Pastor, A. M. & Flores, E. Nitrogen control in cyanobacteria. J. Bacteriol. 183, 411–425 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. 70

    Adler, S., Trapp, E. M., Dede, C., Maier, U. G. & Zauner, S. in Endosymbiosis 167–179 (Springer, 2013).

    Google Scholar 

  71. 71

    Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).

    CAS  PubMed  Google Scholar 

  72. 72

    Kazamia, E., Helliwell, K. E., Purton, S. & Smith, A. G. How mutualisms arise in phytoplankton communities: building eco-evolutionary principles for aquatic microbes. Ecol. Lett. 19, 810–822 (2016).

    PubMed  PubMed Central  Google Scholar 

  73. 73

    Green, B. R. Chloroplast genomes of photosynthetic eukaryotes. Plant J. 66, 34–44 (2011).

    CAS  PubMed  Google Scholar 

  74. 74

    Dyall, S. D., Brown, M. T. & Johnson, P. J. Ancient invasions: from endosymbionts to organelles. Science 304, 253–257 (2004).

    CAS  PubMed  Google Scholar 

  75. 75

    Nakayama, T. & Archibald, J. M. Evolving a photosynthetic organelle. BMC Biol. 10, 35 (2012).

  76. 76

    Nowack, E. C. et al. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol. Biol. Evol. 28, 407–422 (2011).

    CAS  PubMed  Google Scholar 

  77. 77

    Bodyl, A., Mackiewicz, P. & Gagat, P. Organelle evolution: Paulinella breaks a paradigm. Curr. Biol. 22, R304–306 (2012).

    CAS  PubMed  Google Scholar 

  78. 78

    Miyagishima, S. Y. Mechanism of plastid division: from a bacterium to an organelle. Plant Physiol. 155, 1533–1544 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. 79

    Melkonian, M. & Mollenhauer, D. Robert Lauterborn (1869–1952) and his Paulinella chromatophora. Protist 156, 253–262 (2005).

    PubMed  Google Scholar 

  80. 80

    Theissen, U. & Martin, W. The difference between organelles and endosymbionts. Curr. Biol. 16, R1016–R1017 (2006); author reply 16, R1017–R1018 (2006).

    CAS  PubMed  Google Scholar 

  81. 81

    Hilton, J. A. et al. Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont. Nat. Commun. 4, 1767 (2013).

  82. 82

    Church, M. J., Jenkins, B. D., Karl, D. M. & Zehr, J. P. Vertical distributions of nitrogen-fixing phylotypes at Stn ALOHA in the oligotrophic North Pacific Ocean. Aquat. Microb. Ecol. 38, 3–14 (2005).

    Google Scholar 

  83. 83

    Needoba, J. A., Foster, R. A., Sakamoto, C. & Zehr, J. P. Nitrogen fixation by unicellular diazotrophic cyanobacteria in the temperate oligotrophic North Pacific Ocean. Limnol. Oceanogr. 52, 1317–1327 (2007).

    CAS  Google Scholar 

  84. 84

    Foster, R. A. et al. Influence of the Amazon River plume on distributions of free-living and symbiotic cyanobacteria in the western tropical north Atlantic Ocean. Limnol. Oceanogr. 52, 517–532 (2007).

    CAS  Google Scholar 

  85. 85

    Man-Aharonovich, D., Kress, N., Zeev, E. B., Berman-Frank, I. & Béjà, O. Molecular ecology of nifH genes and transcripts in the eastern Mediterranean Sea. Environ. Microbiol. 9, 2354–2363 (2007).

    CAS  PubMed  Google Scholar 

  86. 86

    Hashimoto, R., Yoshida, T., Kuno, S., Nishikawa, T. & Sako, Y. The first assessment of cyanobacterial and diazotrophic diversities in the Japan Sea. Fish. Sci. 78, 1293–1300 (2012).

    CAS  Google Scholar 

  87. 87

    Brown, S. M. & Jenkins, B. D. Profiling gene expression to distinguish the likely active diazotrophs from a sea of genetic potential in marine sediments. Environ. Microbiol. 16, 3128–3142 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88

    Bothe, H., Tripp, H. J. & Zehr, J. P. Unicellular cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed. Arch. Microbiol. 192, 783–790 (2010).

    CAS  PubMed  Google Scholar 

  89. 89

    Heller, P., Tripp, H. J., Turk-Kubo, K. & Zehr, J. P. ARBitrator: a software pipeline for on-demand retrieval of auto-curated nifH sequences from GenBank. Bioinformatics 30, 2883–2890 (2014).

    CAS  PubMed  Google Scholar 

  90. 90

    Messer, L. F. et al. High levels of heterogeneity in diazotroph diversity and activity within a putative hotspot for marine nitrogen fixation. ISME J. 10, 1499–1513 (2016).

    CAS  PubMed  Google Scholar 

  91. 91

    Turk-Kubo, K. A. et al. Diazotroph community succession during the VAHINE mesocosm experiment (New Caledonia lagoon). Biogeosciences 12, 7435–7452 (2015).

    CAS  Google Scholar 

  92. 92

    Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. 93

    Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. 94

    Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95

    Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428, 726–731 (2016).

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank J. Magasin for bioinformatics assistance and the personnel of the Hawaiian Ocean Time Series program. This work supported in part by a grant from the Simons Foundation (SCOPE Award ID 329108, J.P.Z.), and the NSF Center for Microbial Oceanography: Research and Education (C-MORE, DBI no. 0424599). M.M.M. is supported by a Marie Curie International Outgoing Fellowship within the 7th European Community Framework Programme. H.M.F. is supported by the Swedish Research Council VR 637-2013-7502.

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J.P.Z. conceptualized and drafted the manuscript. I.N.S. performed genome comparisons and prepared accompanying figure. M.M.M. compiled photomicrographs, and prepared conceptual figures. K.T.K. performed phylogenetic analysis and prepared accompanying figure. J.P.Z., I.N.S., H.M.F., M.M.M. and K.T.K. drafted and edited the manuscript and figures. All authors read and approved the final manuscript.

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Correspondence to Jonathan P. Zehr.

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Zehr, J., Shilova, I., Farnelid, H. et al. Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A. Nat Microbiol 2, 16214 (2017). https://doi.org/10.1038/nmicrobiol.2016.214

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