Unique genome evolution in an intracellular N2-fixing symbiont of a rhopalodiacean diatom

Takuro Nakayama, Yuji Inagaki

Abstract


Cyanobacteria, the major photosynthetic prokaryotic lineage, are also known as a major nitrogen fixer in nature. N2-fixing cyanobacteria are frequently found in symbioses with various types of eukaryotes and supply fixed nitrogen compounds to their eukaryotic hosts, which congenitally lack N2-fixing abilities. Diatom species belonging to the family Rhopalodiaceae also possess cyanobacterial symbionts called spheroid bodies. Unlike other cyanobacterial N2-fixing symbionts, the spheroid bodies reside in the cytoplasm of the diatoms and are inseparable from their hosts. Recently, the first spheroid body genome from a rhopalodiacean diatom has been completely sequenced. Overall features of the genome sequence showed significant reductive genome evolution resulting in a diminution of metabolic capacity. Notably, despite its cyanobacterial origin, the spheroid body was shown to be truly incapable of photosynthesis implying that the symbiont energetically depends on the host diatom. The comparative genome analysis between the spheroid body and another N2-fixing symbiotic cyanobacterial group corresponding to the UCYN-A phylotypes – both were derived from cyanobacteria closely related to genus Cyanothece – revealed that the two symbionts are on similar, but explicitly distinct tracks of reductive evolution. Intimate symbiotic relationships linked by nitrogen fixation as seen in rhopalodiacean diatoms may help us better understand the evolution and mechanisms of bacterium-eukaryote endosymbioses.

Keywords


nitrogen fixation; endosymbiosis; genome reduction; spheroid body; rhopalodiacean diatom

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References


Kneip C, Lockhart P, Voß C, Maier UG. Nitrogen fixation in eukaryotes – new models for symbiosis. BMC Evol Biol. 2007;7(1):55. http://dx.doi.org/10.1186/1471-2148-7-55

Rai AN, Bergman B, Rasmussen U, editors. Cyanobacteria in symbiosis. Dordrecht: Kluwer Academic Publishers; 2002.

Janson S. Cyanobacteria in symbiosis with diatoms. In: Rai AN, Bergman B, Rasmussen U, editors. Cyanobacteria in symbiosis. Dordrecht: Springer; 2002. p. 1–10. http://dx.doi.org//10.1007/0-306-48005-0_1

Foster RA, Kuypers MMM, Vagner T, Paerl RW, Musat N, Zehr JP. Nitrogen fixation and transfer in open ocean diatom–cyanobacterial symbioses. ISME J. 2011;5(9):1484–1493. http://dx.doi.org/10.1038/ismej.2011.26

Nakayama T, Ikegami Y, Nakayama T, Ishida K, Inagaki Y, Inouye I. Spheroid bodies in rhopalodiacean diatoms were derived from a single endosymbiotic cyanobacterium. J Plant Res. 2011;124(1):93–97. http://dx.doi.org/10.1007/s10265-010-0355-0

Adler S, Trapp EM, Dede C, Maier UG, Zauner S. Rhopalodia gibba: the first steps in the birth of a novel organelle? In: Löffelhardt W, editor. Endosymbiosis. Vienna: Springer; 2014. p. 167–179. http://dx.doi.org/10.1007/978-3-7091-1303-5_9

Round FE, Crawford RM, Mann DG. The diatoms: biology & morphology of the genera. Cambridge: Cambridge University Press; 1990.

Drum RW, Pankratz S. Fine structure of an unusual cytoplasmic inclusion in the diatom genus, Rhopalodia. Protoplasma. 1965;60(1):141–149. http://dx.doi.org/10.1007/BF01248136

Prechtl J. Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol Biol Evol. 2004;21(8):1477–1481. http://dx.doi.org/10.1093/molbev/msh086

Hagino K, Onuma R, Kawachi M, Horiguchi T. Discovery of an endosymbiotic nitrogen-fixing cyanobacterium UCYN-A in Braarudosphaera bigelowii (Prymnesiophyceae). PLoS ONE. 2013;8(12):e81749. http://dx.doi.org/10.1371/journal.pone.0081749

De Yoe HR, Lowe RL, Marks JC. Effects of nitrogen and phosphorus on the endosymbiont load of Rhopalodia gibba and Epithemia turgida (Bacillariophyceae). J Phycol. 1992;28(6):773–777. http://dx.doi.org/10.1111/j.0022-3646.1992.00773.x

Hilton JA, Foster RA, James Tripp H, Carter BJ, Zehr JP, Villareal TA. Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont. Nat Commun. 2013;4:1767. http://dx.doi.org/10.1038/ncomms2748

Kies L. Glaucocystophyceae and other protists harbouring prokaryotic endocytobionts. In: Reisser W, editor. Algae and symbioses. Bristol: Biopress; 1992. p. 353–377.

Nakayama T, Kamikawa R, Tanifuji G, Kashiyama Y, Ohkouchi N, Archibald JM, et al. Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle. Proc Natl Acad Sci USA. 2014;111(31):11407–11412. http://dx.doi.org/10.1073/pnas.1405222111

Kneip C, Voβ C, Lockhart PJ, Maier UG. The cyanobacterial endosymbiont of the unicellular algae Rhopalodia gibba shows reductive genome evolution. BMC Evol Biol. 2008;8(1):30. http://dx.doi.org/10.1186/1471-2148-8-30

Wernegreen JJ. Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet. 2002;3(11):850–861. http://dx.doi.org/10.1038/nrg931

Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S, Harada M, et al. Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr Biol. 2007;17(10):881–886. http://dx.doi.org/10.1016/j.cub.2007.04.039

Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 2008;42(1):165–190. http://dx.doi.org/10.1146/annurev.genet.41.110306.130119

Nowack ECM, Melkonian M, Glöckner G. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol. 2008;18(6):410–418. http://dx.doi.org/10.1016/j.cub.2008.02.051

Bandyopadhyay A, Elvitigala T, Welsh E, Stockel J, Liberton M, Min H, et al. Novel metabolic attributes of the genus Cyanothece, comprising a group of unicellular nitrogen-fixing cyanobacteria. mBio. 2011;2(5):e00214–11. http://dx.doi.org/10.1128/mBio.00214-11

Kanehisa M. The KEGG resource for deciphering the genome. Nucl Acids Res. 2004;32(90001):277D–280. http://dx.doi.org/10.1093/nar/gkh063

Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature. 2000;407(6800):81–86. http://dx.doi.org/10.1038/35024074

Tripp HJ, Bench SR, Turk KA, Foster RA, Desany BA, Niazi F, et al. Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature. 2010;464(7285):90–94. http://dx.doi.org/10.1038/nature08786

Hajós M. Stratigraphy of Hungary’s Miocene diatomaceous Earth deposits. Budapest: Institutum Geologicum Hungaricum; 1986. (Geologica Hungarica; vol 49).

Simonsen R. The diatom system: ideas on phylogeny. Bacillaria. 1979;2:9–71.

Gomez-Valero L. The evolutionary fate of nonfunctional DNA in the bacterial endosymbiont Buchnera aphidicola. Mol Biol Evol. 2004;21(11):2172–2181. http://dx.doi.org/10.1093/molbev/msh232

Zehr JP, Mellon MT, Zani S. New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl Env. Microbiol. 1998;64(9):3444–3450.

Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, et al. Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science. 2008;322(5904):1110–1112. http://dx.doi.org/10.1126/science.1165340

Goebel NL, Turk KA, Achilles KM, Paerl R, Hewson I, Morrison AE, et al. Abundance and distribution of major groups of diazotrophic cyanobacteria and their potential contribution to N2 fixation in the tropical Atlantic Ocean. Environ Microbiol. 2010;12(12):3272–3289. http://dx.doi.org/10.1111/j.1462-2920.2010.02303.x

Bombar D, Heller P, Sanchez-Baracaldo P, Carter BJ, Zehr JP. Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria. ISME J. 2014;8(12):2530–2542. http://dx.doi.org/10.1038/ismej.2014.167

Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N, Vaulot D, et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science. 2012;337(6101):1546–1550. http://dx.doi.org/10.1126/science.1222700