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Capsaspora Owczarzaki The origin of metazoan multicellularity: what comparative genomics is telling us and how we could go forward Iñaki Ruiz-Trillo, Institute of Evolutionary Biology & Universitat de Barcelona & Kitp Cooperation And The Evolution Of Multicellularity, Kitp, 21 February 2013 1 Institut de Biologia Evolutiva (UPF-CSIC) 2 3 3 3 3 last common unicellular ancestor 4 last common unicellular ancestor 4 1. A phylogenetic framework 5 who are the closest living relatives of animals? Fungi Choanoflagellata Metazoa 6 who are the closest living relatives of animals? Fungi Choanoflagellata Metazoa Capsaspora Ministeria Nuclearia Ichthyosporea ? Corallochytrium 6 A new phylogenetic framework Fungi Choanoflagellata Metazoa Holozoa Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2012 Mol Biol Evol 29, 531–544. 7 A new phylogenetic framework Fungi Choanoflagellata Metazoa Nucleariidae Fonticula alba Holozoa Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2012 Mol Biol Evol 29, 531–544. 7 A new phylogenetic framework Fungi Choanoflagellata Metazoa Nucleariidae Filasterea Capsaspora Ministeria Fonticula alba Holozoa Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2012 Mol Biol Evol 29, 531–544. 7 A new phylogenetic framework Fungi Choanoflagellata Metazoa Nucleariidae Filasterea Capsaspora Ministeria Fonticula alba Ichthyosporea Holozoa Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2012 Mol Biol Evol 29, 531–544. 7 2. Genome data 8 M. brevicollis genome Fungi Choanoflagellata Metazoa King et al. 2008 Nature 451:783-788. 9 M. brevicollis genome Fungi Choanoflagellata Metazoa King et al. 2008 Nature 451:783-788. 9 M. brevicollis genome Fungi Choanoflagellata Metazoa cell adhesion (cadherins) cell signaling (protein tyrosine kinases) King et al. 2008 Nature 451:783-788. 9 M. brevicollis genome Fungi Choanoflagellata Metazoa cell adhesion (cadherins) cell signaling (protein tyrosine kinases) integrins WNT pathway TGF-B pathway Notch pathway Hedgehog pathway several TFs King et al. 2008 Nature 451:783-788. 9 Unicellular relatives of animals: not a game of one Fungi Holozoa Choanoflagellata Metazoa Nucleariidae Filasterea Capsaspora Ministeria Fonticula alba Ichthyosporea Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2011 Mol Biol Evol 10 Unicellular relatives of animals: not a game of one Fungi Holozoa Choanoflagellata Metazoa Nucleariidae Filasterea Capsaspora Ministeria Fonticula alba Ichthyosporea Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2011 Mol Biol Evol 10 Unicellular relatives of animals: not a game of one Fungi Holozoa Choanoflagellata Metazoa Nucleariidae Filasterea Capsaspora Ministeria Fonticula alba Ichthyosporea Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2011 Mol Biol Evol 10 Unicellular relatives of animals: not a game of one Fungi Holozoa Choanoflagellata Metazoa Nucleariidae Filasterea Capsaspora Ministeria Fonticula alba Ichthyosporea Ruiz-Trillo et al. 2008 Mol Biol Evol 25:664-672. Shalchian-Tabrizi et al. 2008 PLoS ONE 3:e2098. Brown et al. 2009 Mol Biol Evol 26:2699-2709. Torruella et al. 2011 Mol Biol Evol 10 UNICORN project Fungi Holozoa Allomyces macrogynus Choanoflagellata Salpingoeca Monosiga Spizellomyces Filasterea rosetta brevicollis Metazoa punctatus Capsaspora Ministeria Mortierella owczarzaki vibrans verticillata Ichthyosporea Nucleariidae Sphaeroforma Amoebidium arctica parasiticum Fonticula alba Thecamonas Apusozoa trahens Ruiz-Trillo et al. 2007. Trends in Genetics 23:113-118. 11 UNICORN: sequenced genomes (August 2012) Fungi Allomyces macrogynus Choanoflagellata Monosiga Spizellomyces Salpingoeca Filasterea brevicollis Metazoa punctatus rosetta Capsaspora Ministeria Mortierella owczarzaki vibrans verticillata Ichthyosporea Nucleariidae Sphaeroforma Amoebidium arctica parasiticum Fonticula alba we are responsible for Capsaspora Thecamonas Apusozoa and trahens Sphaeroforma Ruiz-Trillo et al. 2007. Trends in Genetics 23:113-118. 12 Integrin-mediated adhesion system: pre-UNICORN view Amoebozoa Thecamonas Fungi Capsaspora Choanoflagellata Metazoa Salpingoeca Allomyces Monosiga Spizellomyces Batrachochytrium membrane 13 Integrin-mediated adhesion system: post-UNICORN view Amoebozoa Thecamonas Fungi Capsaspora Choanoflagellata Metazoa Allomyces Monosiga Salpingoeca Spizellomyces Batrachochytrium membrane Sebé-Pedrós et al. 2010. PNAS 107:10142-10147. 14 Metazoan Transcription Factors (TFs) Other Other eukaryotes Amoebozoa Amastigomonas fungi Allomyces Spizellomyces Capsaspora Monosiga Metazoa HD: PBC, prd-like. Ets, Smad, NR HD: ANTP, POU, LIM, Irx, Meis. bZIP: PAR, C/EBP, CREB. bZIP: Jun, Fos, Atf3, ... Grainyhead-like bHLH: Groups A, D, E, F. bHLH: MAD, MITF, Class I Fox TFs USF, Mlx, Group C. HMGbox: Sox, TCF/LEF. bZIP: Atf4/5 HMGbox: Sox-like Holozoa Grainyhead-like Runx NFkappaB/Rel p53 bZIP: Oasis, Atf6, CREB, PAR, C/EBP, Atf2. Opisthokonts bHLH: Myc, Max, Mad, USF, Mlx, SREBP, MITF, Group C: ARNT. HD: Pbx, Prd-like. T-box Unikonts Metazoan-like Mef2 CP2 TFs Metazoan-like STAT Fox TFs STAT TFs Churchill Mef2-like (Type II) MAD-box bZIP TFs bHLH TFs HD: TALE, non-TALE HMGbox TFs Sebé-Pedrós et al. 2011. Mol. Biol. Evol. 28:1241-54 15 Metazoan Transcription Factors: pre-UNICORN view Metazoa Capsaspora Choanoflagellata NF-Kappa Thecamonas Monosiga Allomyces Fungi ETS, Smad, NR Grainyhead-like T-box Spizellomyces Amoebozoa Runx p53 other eukaryotes Fox membrane 16 Metazoan Transcription Factors: post-UNICORN view Metazoa Capsaspora Choanoflagellata Thecamonas Monosiga Allomyces Fungi ETS, Smad, NR Spizellomyces Amoebozoa other Grainyhead-like eukaryotes p53 Runx NF-Kappa T-box membrane Fox Sebé-Pedrós et al. 2011. Mol. Biol. Evol. 28:1241-54 17 Capsaspora has a Brachyury gen Brachyury Fungi Co Dtbx1 Dm Bra Filasterea Sd Bra Porifera Hs Tbx19 Om Bra Cnidaria & Ctenophora Pp Bra Nv Bra Co Bra Placozoa Bra Ml Ta Bra Hv Bra2 Bilateria Co Dtbx2 Hs T Pc Bra Sr Bra Hv Bra1He Bra Aq Tbx1/15/20 Av Tbx1/15/20 Sp Tbx 100/1.00 60/0.98 50/0.98 Tbx2/3 64/1.00 Tbr Dm bi 34/0.84 Hs Tbx21HsEomes Pp Tbx2/3 Ta Tbx2/3 Hs Tbx3 100/1.00 Hs Tbr1 ! Nv Tbx2/3 Hs Tbx2 d Ml Tbx2/3 77/1.00 -/0.90 -/- -/1.00 Aq TbxA Aq TbxE Hs Tbx15 Nv Tbx20 67/0.99 85/1.00 Aq TbxC Hs Tbx18 41/1.00 Aq TbxD Hs Tbx22 Nv Tbx20.3 Hs Tbx6 Hs Tbx5 Hs Tbx4 Hs MGA Nv Tbx20.2 Hs Tbx20 PcTbx4/5 Dm dc2 AqTbx4/5 Dm dc1 Ml Tbx1 Dm dc3 Dm midline Nv Tbx1p Tbx2 Sd Tbx6 Aq TbxB Dm H15 Hs Tbx1 Nv Tbx4/5 Nv Tbx1 Nv Tbx20.1 Dm org-1 Tbx1/15/20 Hs Tbx10 Tbx4/5 Co Tbx3 0.4 Sebé-Pedrós et al. 2011. Mol. Biol. Evol. 28:1241-54 18 PFAM gain/loss a i k b [Gain] Gene Ontology N domains za ollis r c Holozoa Signal transducer activity 8 oa i z evi cza Transcription regulatory region DNA binding 7 r w g eta o un Metazoa Extracellular region 9 . F M M. b C Outgroup Transcription regulatory region DNA binding 8 c [Loss] 5157 3014 3287 3941 +235 +19 +6 +55 Holozoa Hydrolase activity (O-glycosyl bonds) 7 -56 -1983 -1688 -1143 Fungi Multi-organism process 10 Negative regulation of hydrolase activity 7 Transcription regulatory region DNA binding 16 Metazoa+ 4978 Choano +61 M. brevicollis Extracellular region 29 -52 Regulation of transcription, DNA-dependent 62 Nucleoplasm 22 Holozoa 4969 Developmental process 11 +100 Cellular cell wall organization or biogenesis 7 -160 Racemase and epimerase activity 8 C. owczarzaki Extracellular region 26 5029 Opisthokonta Receptor binding 12 Reproduction 12 Multicellular organismal process 13 Cell wall organization biogenesis 11 Pathogenesis 8 Viral reproduction 9 External encapsulating structure 7 19 Figure 2. Suga et al. PFAM gain/loss a i k b [Gain] Gene Ontology N domains za ollis r c Gains (geneHolozoa ontology,Signal transdu >cer 7 a domainsctivity ) 8 oa i z evi cza Transcription regulatory region DNA binding 7 r w g eta o un HolozoaMetazoa Extracellular region 9 . F M M. b C Outgroup Transcription regulatory region DNA binding 8 Signal transducer activity c [Loss]Transcription regulatory 5157 3014 3287 3941 +235 +19 +6 +55 regionHolozoa DNAHydrolase binding activity (O-glycosyl bonds) 7 -56 -1983 -1688 -1143 Fungi Multi-organism process 10 Negative regulation of hydrolase activity 7 Transcription regulatory region DNA binding 16 Metazoa+ 4978 Choano +61 M. brevicollis Extracellular region 29 -52 Regulation of transcription, DNA-dependent 62 Nucleoplasm 22 Holozoa 4969 Developmental process 11 +100 Cellular cell wall organization or biogenesis 7 -160 Racemase and epimerase activity 8 C. owczarzaki Extracellular region 26 5029 Opisthokonta Receptor binding 12 Reproduction 12 Multicellular organismal process 13 Cell wall organization biogenesis 11 Pathogenesis 8 Viral reproduction 9 External encapsulating structure 7 19 Figure 2. Suga et al. PFAM gain/loss a i k b [Gain] Gene Ontology N domains za ollis r c Gains (geneHolozoa ontology,Signal transdu >cer 7 a domainsctivity ) 8 oa i z
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