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Ecotypic diversity of marine cyanobacteria: Tales from the pangenome

Ecotypic diversity of marine cyanobacteria: Tales from the pangenome. Gabrielle Rocap. Small (0.6 x 0.8 m m) divinyl chlorophylls a and b. Larger (0.8 x 1.8 m m) phycobilisomes. Unicellular marine cyanobacteria. ubiquitous throughout the tropical and sub tropical oceans

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Ecotypic diversity of marine cyanobacteria: Tales from the pangenome

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  1. Ecotypic diversity of marine cyanobacteria: Tales from the pangenome Gabrielle Rocap

  2. Small (0.6 x 0.8 mm) divinyl chlorophylls a and b Larger (0.8 x 1.8 mm) phycobilisomes Unicellular marine cyanobacteria • ubiquitous throughout the tropical and sub tropical oceans • extremely abundant (up to 4x105 cells/ml) • contribute significantly to primary productivity Prochlorococcus Synechococcus Images from http://ccmp.bigelow.org

  3. Prochlorococcus and Synechococcus have differing seasonal abundances in the Sargasso Sea Durand et al., Deep Sea Research II 2001

  4. 2 MIT9312 MIT9313 Chl b/chl a2 1 0 1 10 100 1000 Growth Irradiance (mol Q m-2 s-1) Prochlorococcus isolates differ in their photophysiology 1 MIT9312 0.8 Growth rate (day-1) 0.6 MIT9313 0.4 0.2 0 1 10 100 1000 Growth irradiance (mol Q m-2 s-1) From Moore, Rocap & Chisholm 1998

  5. rRNA phylogeny corresponds to physiological differences —”ecotypes” ENATL6 ENATL2 NATL2 I ENATL5 SAR6 TATL1a MED4 89 ENATL1 ENATL3 97 MIT9302 MIT9312 MIT9201 92 II GP2 MIT9202 71 MIT9215 TATL1b MIT9107 66 NATL2A I 100 PAC1 78 ENATL7 ENATL4 II SS120 72 MIT9211 III MIT9303 IV MIT9313 SAR139 WH8112 84 WH8102 Marine Synechococcus SAR100 WH8101 WH8012 WH7805 SAR7 Cyanobium PCC 6307 Adapted from Rocap et al 1999 0.01

  6. Prochlorococcusecotypes partition the water column Ahlgren et al 2005 Env. Micro.

  7. 40°S 20°S 0° 20°N 40°N Prochlorococcusecotypes have latitudinal gradients Johnson et al. Nature 2006

  8. Whole genome sequences reveal large differences among strains ENATL6 ENATL2 NATL2 ENATL5 SAR6 TATL1a 1.66 Mbp, 31 %G+C MED4 89 ENATL1 ENATL3 97 MIT9302 MIT9312 MIT9201 92 GP2 MIT9202 71 MIT9215 TATL1b MIT9107 66 NATL2A 100 PAC1 78 ENATL7 ENATL4 1.75 Mbp, 36 %G+C SS120 72 MIT9211 MIT9303 2.41 Mbp, 51 %G+C MIT9313 SAR139 WH8112 84 2.43 Mbp, 60 %G+C WH8102 SAR100 WH8101 WH8012 WH7805 SAR7 Cyanobium PCC 6307 0.01

  9. Protein Family domains in 3 Prochlorococcus genomes 11 SS120 (low light) 24 MED4 (high light) 30 865 35 21 119 MIT9313 (low light)

  10. 21 domains in MED4 and MIT9313 but not SS120 include: Urease_alpha Urease alpha-subunit, N-terminal domain Urease_beta Urease beta subunit Urease_gamma Urease, gamma subunit UreD UreD urease accessory protein UreE_C UreE urease accessory protein, C-terminal domain UreF UreF ureC ureB ureA ureD ureE ureF ureG urtA urtB urtC urtD urtE

  11. 30 domains in MED4 but not SS120 or MIT9313 include: Cyanate lyase Cyanate lyase-C-terminal domain cynS Cyanate ABC transporter

  12. 119 domains in MIT9313 but not SS120 or MED4 include: Form_nir_trans Formate/Nitrite transporter

  13. Synechococcus WH8102 narB nirA Prochlorococcus MIT9313 nirA Prochlorococcus MED4 deletion deletion Rocap et al 2003 Nature

  14. Summary of N source utilization genes • NH4 • NO2 • NO3 • urea • cyanate • N2 MED4 + - - + + - SS120 + - - - - - MIT9313 + + - + - -

  15. What is the interplay between “core” and “unique” genes in determining ecotype fitness?

  16. MIT9301 AS9601 MIT9312 MIT9515 MED4 NATL1A NATL2A SS120 MIT9303 MIT9313 WH7803 WH7805 CC9311 RS9916 RS9917 CC9902 BL107 CC9605 WH8102 RCC307 WH5701 0.1 21 genomes now available High light Prochlorococcus Low light coastal oligotrophic motile oligotrophic Synechococcus coastal ? coastal ? coastal ? coastal

  17. Defining the marine cyanobacterial core: Orthologs defined by reciprocal best blast hits Paralogs resolved by a combination of computational and manual curation 1082

  18. 3500 3000 unilogs 2500 2000 core 1500 2-20 orthologs 1000 500 0 MED4 RS9917 RS9916 AS9601 CC9311 CC9605 CC9902 RCC307 BL107 SS120 WH5701 WH7805 WH7803 WH8102 NATL2A NATL1A MIT9313 MIT9303 MIT9301 MIT9312 MIT9515 Core genes make up only 40-60% of each genome Number of genes eMIT9313 eMIT9312 eMED4 clade 4 eNATL2A Ahlgren & Rocap in prep Low light Pro High light Pro Synechococcus

  19. The pan genome is dominated by unilogs COG categories core 9% 27% 2-20 orthologs 64 % unilogs Colored pie portions: assignable COG function Unknown function Ahlgren & Rocap in prep

  20. Phylogenomics of core genes Find tree for each gene set Ask: Are there genes with evolutionary distances that are greater than or smaller than avergage? Ask: Are there trees with conflicting branching order suggesting horizontal transfer of some genes? consensus

  21. 0.14 0.12 0.1 0.08 25 1 23 0.06 22 21 20 0.04 17 3 0.02 4 1 6 16 9 0 25 3 15 0 3 6 9 12 15 18 21 24 27 30 4 5 8 9 1 3 10 4 24 14 6 23 15 10 18 22 19 16 21 17 20 20 19 18 25 22 24 Relative rates of evolution vary among core genes COG classification Slow core genes 1 Translation, ribosome 4 Replication, recombination, repair All core genes n=1082 15 Chaperones, protein modification 16 Energy product and conversion 20 Coenzyme transport and metabolism 25 Unknown function frequency Fast core genes total protein tree distance Ahlgren & Rocap in prep

  22. MIT9301 Genome reductions AS9601 MIT9312 NATL1A MIT9515 NATL2A SS120 MIT9303 MIT9313 MED4 CC9902 BL107 CC9605 WH8102 RCC307 WH5701 0.1 Gene gains (non-unilog) Unilog gains WH7803 Gene losses WH7805 CC9311 RS9916 RS9917 MIT9515 MED4 Phylogenetic mapping of gene gain/loss events High light Pro MIT9301 AS9601 MIT9312 NATL2A Low light Pro NATL1A SS120 MIT9313 MIT9303 CC9902 BL107 Cluster 1 Syn CC9605 WH8102 RS9916 RS9917 Cluster 2 Syn WH7805 WH7803 CC9311 RCC307 WH5701 Ahlgren & Rocap in prep

  23. RS9916 RS9916 RS9917 RS9917 WH7805 WH7805 WH7803 WH7803 CC9311 CC9311 CC9902 CC9902 BL107 BL107 CC9605 CC9605 WH8102 WH8102 MIT9313 MIT9313 MIT9303 MIT9303 NATL2A NATL2A NATL1A NATL1A MIT9515 MIT9515 MED4 MED4 MIT9301 MIT9301 AS9601 AS9601 MIT9312 MIT9312 SS120 RCC307 RCC307 WH5701 WH5701 Function of genes gained Selected COG categories Replication Amino acid transport & metab. 2’ metabolite transp. & metab. Carbohydrate transport & metab. Transduction Inorganic ion transport & metab. Defense mechanisms Ahlgren & Rocap in prep Cell wall/membrane biogenesis All other functions

  24. tRNA Gly MED4 mutS gyrB secA cysE PMM1645 PMM1634 13,648 bp tRNA Gly MIT 9313 mutS gyrB secA cysE PMT0079 PMT0121 56,445 bp tRNA Gly mutS gyrB WH 8102 cysE secA WH0078 WH0095 22,507 bp 67 MIT 9313 51 %G+C 27 Insertions of cell surface gene clusters 33 gene insertion

  25. MIT9515 MIT9515 MED4 MED4 MIT9301 MIT9301 AS9601 AS9601 MIT9312 MIT9312 NATL2A NATL2A NATL1A NATL1A SS120 MIT9313 MIT9313 MIT9303 MIT9303 CC9902 CC9902 BL107 BL107 CC9605 CC9605 WH8102 WH8102 RS9916 RS9916 RS9917 RS9917 WH7805 WH7805 WH7803 WH7803 CC9311 CC9311 RCC307 RCC307 WH5701 WH5701 Function of genes lost Selected COG categories Replication Amino acid transport & metab. 2’ metabolite transp. & metab. Carbohydrate transport & metab. Transduction Inorganic ion transport & metab. Defense mechanisms Ahlgren & Rocap in prep Cell wall/membrane biogenesis All other functions

  26. Where do the unilogs come from? Crenarchaeota Euryarchaeota phage Acidobacteria Actinobacteria Bacteroidetes Chlamydiae Chlorobi Cyanobacteria Deinococcus-Thermus Firmicutes Planctomycetes Alphaproteobacteria Betaproteobacteria Deltaproteobacteria Epsilonproteobacteria Gammaproteobacteria Magnetococcus Spirochaetes Possible duplication events phage: 0.15% 23% Archaea: 0.3% Bacteria: 9% 68% ORFans n = 7241 n = 963

  27. Genomic islands Coleman et al. 2006, Science

  28. No genes have an ortholog in subject All genes have an ortholog in subject Found in all genomes(core) Found only in query (unilog)

  29. RCC307 RS9917 RS9916 CC9311 WH7803 BL107 CC9902 Synechococcus WH8102 Isl. 7 Isl. 4 Island 3, insertion of capsular polysaccharide synthesis. Isl. 18 Islands 36: nitrate operon deleted in RS9917 Isl. 19 Isl. 37 % GC tRNAs Islands 33,34: urea operon deleted in WH7803 Inverted and direct repeats Genomic island Island 29: phycobilisome genes deleted in RS9917 Found in all genomes(core) No genes have an ortholog in subject (query, WH8102) CC9605 All genes have an ortholog in subject Found only in query (unilog)

  30. Ahlgren & Rocap in prep

  31. “close with a profound quote” How’s your ma? Not too good, she’s on her way out We all are, act accordingly

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