Lifestyle evolution in cyanobacterial symbionts of sponges

mBio

Volumn 6, Issue 3, 2015, Pages

  Burgsdorf, Ilia ^a   Slaby, Beate M ^b   Handley, Kim M ^c,h   Haber, Markus ^a   Blom, Jochen ^d   Marshall, Christopher W ^e   Gilbert, Jack A ^c,e,f,g   Hentschel, Ute ^b   Steindler, Laura ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF CHICAGO   (United States)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

^e ARGONNE NATIONAL LABORATORY   (United States)

^f MARINE BIOLOGICAL LABORATORY   (United States)

^g ZHEJIANG UNIVERSITY   (China)

^h UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ION; METHIONINE; O ANTIGEN; RNA 16S; SIDEROPHORE; PHOTOSYSTEM II;

ARTICLE; BACTERIAL GENOME; BIOGENESIS; CANDIDATUS SYNECHOCOCCUS SPONGIARUM; CELL WALL; CLADISTICS; CONTROLLED STUDY; CYANOBACTERIUM; DNA MODIFICATION; DNA RECOMBINATION; EVOLUTION; GENETIC CODE; INTRASPECIFIC VARIATION; ION TRANSPORT; IRON TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYSTEM II; PREDATION; PRIORITY JOURNAL; PROCHLOROCOCCUS; SIGNAL TRANSDUCTION; SPECIES DIVERSITY; SPONGE (PORIFERA); SYMBIONT; ANIMAL; BACTERIOPHAGE; CLASSIFICATION; DNA SEQUENCE; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY; SEQUENCE ALIGNMENT; SYMBIOSIS; SYNECHOCOCCUS;

CYANOBACTERIA; SYNECHOCOCCUS; SYNECHOCOCCUS SPONGIARUM;

ANIMALS; BACTERIOPHAGES; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; METHIONINE; O ANTIGENS; PHOTOSYSTEM II PROTEIN COMPLEX; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SYMBIOSIS; SYNECHOCOCCUS;

EID: 84936971845     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00391-15     Document Type: Article

References (84)

1. Rubin M, Berman-Frank I, Shaked Y. 2011. Dust-and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium. Nat Geosci 4:529-534. http://dx.doi.org/10.1038/ngeo1181.
2. Larsson J, Nylander JA, Bergman B. 2011. Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol 11:187. http://dx.doi.org/10.1186/1471-2148-11-187.
3. Crispim CA, Gaylarde CC. 2005. Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1-9.
4. Steindler L, Huchon D, Avni A, Ilan M. 2005. 16S rRNA phylogeny of sponge-associated cyanobacteria. Appl Environ Microbiol 71:4127-4131. http://dx.doi.org/10.1128/AEM.71.7.4127-4131.2005.
5. Thacker RW, Freeman CJ. 2012. Sponge-microbe symbioses: recent advances and new directions. Adv Mar Biol 62:57-111. http://dx.doi.org/ 10.1016/B978-0-12-394283-8.00002-3.
6. Honda D, Yokota A, Sugiyama J. 1999. Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48:723-739. http://dx.doi.org/10.1007/PL00006517.
7. UsherKM. 2008. The ecology and phylogeny of cyanobacterial symbionts in sponges. Mar Ecol 29:178-192. http://dx.doi.org/10.1111/j.1439-0485.2008.00245.x.
8. Burgsdorf I, Erwin PM, López-Legentil S, Cerrano C, Haber M, Frenk S, Steindler L. 2014. Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. Front Microbiol 5:529. http://dx.doi.org/10.3389/ fmicb.2014.00529.
9. Erwin PM, López-Legentil S, Turon X. 2012. Ultrastructure, molecular phylogenetics, and chlorophyll a content of novel cyanobacterial symbionts in temperate sponges. Microb Ecol 64:771-783. http://dx.doi.org/ 10.1007/s00248-012-0047-5.
10. Usher KM, Kuo J, Fromont J, Sutton DC. 2001. Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461:15-23. http://dx.doi.org/10.1023/ A:1012748727678.
11. Oren M, Steindler L, Ilan M. 2005. Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraeus. Mar Biol 148:35-41. http://dx.doi.org/ 10.1007/s00227-005-0064-8.
12. Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U. 2008. Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microbiol 74:7694-7708. http://dx.doi.org/10.1128/ AEM.00878-08.
13. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S, Horn M, WagnerM. 2010. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12:2070-2082. http://dx.doi.org/10.1111/j.1462-2920.2009.02065.x.
14. Gao Z-M, Wang Y, Tian R-M, Wong YH, Batang ZB, Al-Suwailem AM, Bajic VB, Qian P-Y. 2014. Symbiotic adaptation drives genome streamlining of the cyanobacterial sponge symbiont "Candidatus Synechococcus spongiarum". mBio 5:e00079-14. http://dx.doi.org/10.1128/mBio.00079-14.
15. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, Sugahara J, Preston C, de la Torre J, Richardson PM, DeLong EF. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad SciUSA103:18296-18301. http://dx.doi.org/ 10.1073/pnas.0608549103.
16. Kamke J, Sczyrba A, Ivanova N, Schwientek P, Rinke C, Mavromatis K, Woyke T, Hentschel U. 2013. Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges. ISME J 7:2287-2300. http://dx.doi.org/10.1038/ismej.2013.111.
17. Tian R-M, Wang Y, Bougouffa S, Gao Z-M, Cai L, Bajic V, Qian P-Y. 2014. Genomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur-oxidizing bacterium in sponge. Environ Microbiol 16:3548-3561. http://dx.doi.org/10.1111/1462-2920.12586.
18. Freeman CJ, Thacker RW. 2011. Complex interactions between marine sponges and their symbiotic microbial communities. Limnol Oceanogr 56:1577-1586. http://dx.doi.org/10.4319/lo.2011.56.5.1577.
19. Freeman CJ, Thacker RW, Baker DM, Fogel ML. 2013. Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance? ISME J 7:1116-1125. http:// dx.doi.org/10.1038/ismej.2013.7.
20. Wu M, Eisen JA. 2008. A simple, fast, and accurate method of phylogenomic inference. Genome Biol 9:R151. http://dx.doi.org/10.1186/gb-2008-9-10-r151.
21. Blom J, Albaum SP, Doppmeier D, Pühler A, Vorhölter F-J, Zakrzewski M, Goesmann A. 2009. Edgar: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10:154. http:// dx.doi.org/10.1186/1471-2105-10-154.
22. Aziz RK, Bartels D, Best A, 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. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75.
23. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, Heidelberg KB, Egan S, Steinberg PD, Kjelleberg S. 2010. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4:1557-1567. http://dx.doi.org/10.1038/ ismej.2010.74.
24. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, Thomas T. 2012. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci U S A 109:E1878-E1887. http://dx.doi.org/10.1073/pnas.1203287109.
25. Snel B, Lehmann G, Bork P, Huynen MA. 2000. STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res 28:3442-3444. http://dx.doi.org/10.1093/nar/ 28.18.3442.
26. Snyder DS, Brahamsha B, Azadi P, Palenik B. 2009. Structure of compositionally simple lipopolysaccharide from marine Synechococcus. J Bacteriol 191:5499-5509. http://dx.doi.org/10.1128/JB.00121-09.
27. Nowack EC, Melkonian M, Glöckner G. 2008. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18:410-418. http://dx.doi.org/10.1016/ j.cub.2008.02.051.
28. Cai F, Axen SD, Kerfeld CA. 2013. Evidence for the widespread distribution of CRISPR-Cas system in the phylum Cyanobacteria. RNA Biol 10:687-693. http://dx.doi.org/10.4161/rna.24571.
29. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV. 2011. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9:467-477. http://dx.doi.org/10.1038/ nrmicro2577.
30. Bombar D, Heller P, Sanchez-Baracaldo P, Carter BJ, Zehr JP. 2014. Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria. ISME J 8:2530-2542. http://dx.doi.org/10.1038/ismej.2014.167.
31. Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T. 2012. Metaproteogenomic analysis of a community of sponge symbionts. ISME J 6:1515-1525. http://dx.doi.org/10.1038/ismej.2012.1.
32. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, McGraw Ea, Martin W, Esser C, Ahmadinejad N, Wiegand C, Madupu R, Beanan MJ, Brinkac LM, Daugherty SC, Durkin S. Kolonay JF, Nelson WC, Mohamoud Y, Lee P, Berry K, Young MB, Utterback T, Weidman J, Nierman WC, Paulsen IT, Nelson KE, Tettelin H, O'Neill SL, Eisen JA. 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2:E69.
33. Moliner C, Fournier P-E, Raoult D. 2010. Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol Rev 34:281-294. http://dx.doi.org/10.1111/j.1574-6976.2010.00209.x.
34. Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ. 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480:241-244. http://dx.doi.org/10.1038/ nature10571.
35. Evdokimov AG, Anderson DE, Routzahn KM, Waugh DS. 2001. Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit. J Mol Biol 312:807-821. http://dx.doi.org/10.1006/jmbi.2001.4973.
36. Marino M, Braun L, Cossart P, Ghosh P. 1999. Structure of the InlB leucine-rich repeats, a domain that triggers host cell invasion by the bacterial pathogen L. monocytogenes. Mol Cell 4:1063-1072. http:// dx.doi.org/10.1016/S1097-2765(00)80234-8.
37. Nguyen MT, Liu M, Thomas T. 2014. Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis. Mol Ecol 23: 1635-1645. http://dx.doi.org/10.1111/mec.12384.
38. Weinberger AD, Sun CL, Pluciński MM, Denef VJ, Thomas BC, Horvath P, Barrangou R, Gilmore MS, Getz WM, Banfield JF. 2012. Persisting viral sequences shape microbial CRISPR-based immunity. PLOS Comput B i o l 8 : e 1 0 0 2 4 7 5 . h t t p : / / d x . d o i . o r g / 1 0 . 1 3 7 1 / journal.pcbi.1002475.
39. Tripp HJ, Bench SR, Turk KA, Foster RA, Desany BA, Niazi F, Affourtit JP, Zehr JP. 2010. Metabolic streamlining in an open-ocean nitrogenfixing cyanobacterium. Nature 464:90-94. http://dx.doi.org/10.1038/ nature08786.
40. Kwan JC, Donia MS, Han AW, Hirose E, Haygood MG, Schmidt EW. 2012. Genome streamlining and chemical defense in a coral reef symbiosis. Proc Natl Acad SciUSA109:20655-20660. http://dx.doi.org/10.1073/ pnas.1213820109.
41. Sveshnikov D, Funk C, Schröder WP. 2007. The PsbP-like protein (sll1418) of Synechocystis sp. PCC 6803 stabilises the donor side of photosystem II. Photosynth Res 93:101-109. http://dx.doi.org/10.1007/s11120-007-9171-3.
42. Usher KM, Kuo J, Fromont J, Toze S, Sutton DC. 2006. Comparative morphology of five species of symbiotic and non-symbiotic coccoid cyanobacteria. Eur J Phycol 41:179-188. http://dx.doi.org/10.1080/ 09670260600631352.
43. Meetam M, Keren N, Ohad I, Pakrasi HB. 1999. The PsbY protein is not essential for oxygenic photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 121:1267-1272. http://dx.doi.org/10.1104/ pp.121.4.1267.
44. Latifi A, Ruiz M, Zhang C-C. 2009. Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258-278. http://dx.doi.org/10.1111/j.1574-6976.2008.00134.x.
45. Lerouge I, Vanderleyden J. 2002. O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev 26:17-47.
46. Pile A, Patterson M, Witman J. 1996. In situ grazing on plankton Mycale lingua. Mar Ecol Prog Ser 141:95-102. http://dx.doi.org/10.3354/ meps141095.
47. Wilkinson CR. 1978. Microbial associations in sponges. III. Ultrastructure of the in situ associations in coral reef sponges. Mar Biol 49:177-185. http://dx.doi.org/10.1007/BF00387117.
48. Wilkinson CR, Garrone R, Vacelet J. 1984. Marine sponges discriminate between food bacteria and bacterial symbionts: electron microscope radioautography and in situ evidence. Proc R Soc London Ser B Biol Sci 220:519-528. http://dx.doi.org/10.1098/rspb.1984.0018.
49. Wehrl M, Steinert M, Hentschel U. 2007. Bacterial uptake by the marine sponge Aplysina aerophoba. Microb. Ecol 53:355-365. http://dx.doi.org/ 10.1007/s00248-006-9090-4.
50. Simkovsky R, Daniels EF, Tang K, Huynh SC, Golden SS, Brahamsha B. 2012. Impairment of O-antigen production confers resistance to grazing in a model amoeba-cyanobacterium predator-prey system. Proc Natl Acad Sci U S A 109:16678-16683. http://dx.doi.org/10.1073/ pnas.1214904109.
51. Marston MF, Pierciey FJ, Shepard A, Gearin G, Qi J, Yandava C, Schuster SC, Henn MR, Martiny JB. 2012. Rapid diversification of coevolving marine Synechococcus and a virus. Proc Natl Acad Sci U S A 109:4544-4549. http://dx.doi.org/10.1073/pnas.1120310109.
52. Albers E. 2009. Metabolic characteristics and importance of the universal methionine salvage pathway recycling methionine from 5=-methylthioadenosine. IUBMB Life 61:1132-1142. http://dx.doi.org/ 10.1002/iub.278.
53. KösterW. 2001. ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B 12. Res Microbiol 152:291-301. http://dx.doi.org/ 10.1016/S0923-2508(01)01200-1.
54. Hopkinson BM, Morel FM. 2009. The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22:659-669. http://dx.doi.org/10.1007/s10534-009-9235-2.
55. Stoddard LI, Martiny JB, Marston MF. 2007. Selection and characterization of cyanophage resistance in marine Synechococcus strains. Appl Environ Microbiol 73:5516-5522. http://dx.doi.org/10.1128/ AEM.00356-07.
56. Fieseler L, Quaiser A, Schleper C, Hentschel U. 2006. Analysis of the first genome fragment from the marine sponge-associated, novel candidate phylum Poribacteria by environmental genomics. Environ Microbiol 8:612-624. http://dx.doi.org/10.1111/j.1462-2920.2005.00937.x.
57. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to singlecell sequencing. J Comput Biol 19:455-477.
58. Alneberg J, Bjarnason BS, de Bruijn I, Schirmer M, Quick J, Ijaz UZ, Lahti L, Loman NJ, Andersson AF, Quince C. 2014. Binning metagenomic contigs by coverage and composition. Nat Methods 11: 1144-1150. http://dx.doi.org/10.1038/nmeth.3103.
59. Darling AE, Jospin G, Lowe E, Matsen FA, Bik HM, Eisen JA. 2014. PhyloSift: phylogenetic analysis of genomes and metagenomes. PEER J 2:e243. http://dx.doi.org/10.7717/peerj.243.
60. Huang Y, Gilna P, Li W. 2009. Identification of ribosomal RNA genes in metagenomic fragments. BioInformatics 25:1338-1340. http:// dx.doi.org/10.1093/bioinformatics/btp161.
61. Peng Y, Leung HC, Yiu SM, Chin FY. 2012. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28:1420-1428. http://dx.doi.org/10.1093/ bioinformatics/bts174.
62. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. http://dx.doi.org/10.1186/ 1471-2105-11-119.
63. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH. 2007. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23:1282-1288. http://dx.doi.org/10.1093/bioinformatics/btm098.
64. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/ bioinformatics/btq461.
65. Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP, Banfield JF. 2009. Community-wide analysis of microbial genome sequence signatures. Genome Biol 10:R85. http://dx.doi.org/10.1186/gb-2009-10-8-r85.
66. Handley KM, VerBerkmoes NC, Steefel CI, Williams KH, Sharon I, Miller CS, Frischkorn KR, Chourey K, Thomas BC, Shah MB, Long PE, Hettich RL, Banfield JF. 2013. Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community. ISME J 7:800-816. http://dx.doi.org/10.1038/ismej.2012.148.
67. Darling AC, Mau B, Blattner FR, Perna NT. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394-1403. http://dx.doi.org/10.1101/gr.2289704.
68. 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. 2013. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42: D206-D214. http://dx.doi.org/10.1093/nar/gkt1226.
69. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41. http://dx.doi.org/10.1186/1471-2105-4-41.
70. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Res 32: D277-D280. http://dx.doi.org/10.1093/nar/gkh063.
71. Wu S, Zhu Z, Fu L, Niu B, Li W. 2011. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics 12:444. http://dx.doi.org/10.1186/1471-2164-12-444.
72. Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH. 2013. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 31:533-538.
73. Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, Jensen LJ, von Mering C, Bork P. 2012. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40:D284-D289. http:// dx.doi.org/10.1093/nar/gkr1060.
74. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. 2014. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30: 3123-3124. http://dx.doi.org/10.1093/bioinformatics/btu494.
75. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. http:// dx.doi.org/10.1093/nar/gkh340.
76. Felsenstein J. 1995. PHYLIP: phylogeny inference package, version 3.57c. Seattle Department of Genetic. University of Washington.
77. Grissa I, Vergnaud G, Pourcel C. 2007. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52-W57. http://dx.doi.org/10.1093/nar/gkm360.
78. Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF. 2011. EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol 12:R44. http:// dx.doi.org/10.1186/gb-2011-12-5-r44.
79. Nübel U, Garcia-Pichel F, Muyzer G. 1997. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327-3332.
80. Iteman I, Rippka R, Tandeau De Marsac N, Herdman M. 2000. Comparison of conserved structural and regulatory domains within divergent 16S rRNA-23S rRNA spacer sequences of cyanobacteria. Microbiology 146:1275-1286.
81. Rocap G, Distel DL, Waterbury JB, Chisholm SW. 2002. Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68: 1180-1191. http://dx.doi.org/10.1128/AEM.68.3.1180-1191.2002.
82. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
83. Dufresne A, Ostrowski M, Scanlan DJ, Garczarek L, Mazard S, Palenik BP, Paulsen IT, de Marsac NT, Wincker P, Dossat C, Ferriera S, Johnson J, Post AF, Hess WR, Partensky F. 2008. Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biol 9:R90. http://dx.doi.org/10.1186/gb-2008-9-5-r90.
84. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. 2011. BLAST Ring image generator (Brig): simple prokaryote genome comparisons. BMC Genomics 12:402. http://dx.doi.org/10.1186/1471-2164-12-402.