Evolution of metazoan genome architecture

We study major transitions in metazoan evolution from the perspective of the underlying genomic changes. Over the past years, we have contributed to the broader sampling of metazoan genomes, revealing ancestral metazoan and bilaterian genomic architectures and their diversification patterns. While we can trace back many gene families to the ancient metazoan ancestor, we also find many of them linked at both micro- (local gene cluster) and macro-syntenic (chromosomal) levels. The functional significance of most of those linkages during development is unknown. Having a broad phylogenetic focus we aim to (1) characterize and expand our knowledge of conserved and novel gene linkages and their associated (non-coding) elements across metazoans, (2) study their evolutionary dynamics through comparative genomics and modeling approaches, and (3) establishing molecular tools for investigating their role during development and clade-specific innovation. Inspired by the analysis of the octopus genome, current research focuses on characterizing the genomes of other cephalopod species, in particular investigating the gene linkage and repetitive element dynamics and their role in the emergence of cephalopod novelties. We are also contributing to the functional study of gene linkages in an emerging cephalopod model system Euprymna scolopes (Hawaiian bobtail squid) and the cnidarian hydra (Hydra magnipapillata).

Oleg Simakov studied Biology and obtained the Diploma degree at the University of Heidelberg, conducting his Diploma research in the group of Daniel Rokhsar at the University of California, Berkeley.

In 2013 he obtained his PhD working in the group of Detlev Arendt at EMBL Heidelberg. The work was conducted as a part of the EMBL International PhD Programme and co-supervised by Axel Meyer at the University of Konstanz, Germany.

In 2013 he worked as a research assistant in the group of Thomas Holstein, University of Heidelberg, followed by a postdoctoral appointment at the Okinawa Institute of Science and Technology Molecular Genetics Unit (led by Sydney Brenner and Daniel Rokhsar).

Since 2017 he is a tenure-track group leader at the University of Vienna

Currently, we are looking for a PhD student and postdocs! Contact: oleg.simakov@univie.ac.at

Oleg Simakov, Wai Yee Wong, Elena Ritschard, Hannah Schmidbaur, Nicolas Robert

 

Selected Publications

Zimmermann B, Robert NSM, Technau U, Simakov O*. Ancient animal genome architecture reflects cell type identities. Nat Ecol Evol. 2019 Aug 5. doi:10.1038/s41559-019-0946-7.

Belcaid M, Casaburi G, McAnulty SJ, Schmidbaur H, Suria AM, Moriano-Gutierrez S, Pankey MS, Oakley TH, Kremer N, Koch EJ, Collins AJ, Nguyen H, Lek S, Goncharenko-Foster I, Minx P, Sodergren E, Weinstock G, Rokhsar DS, McFall-Ngai M, Simakov O*, Foster JS*, Nyholm SV*. Symbiotic organs shaped by distinct modes of genome evolution in cephalopods. Proc Natl Acad Sci USA. 2019 Feb 19;116(8):3030-3035. doi: 10.1073/pnas.1817322116. (cover)

Simakov O*, Kawashima T. Independent evolution of genomic characters during major metazoan transitions. Dev Biol. 2017 Jul 15;427(2):179-192. doi:10.1016/j.ydbio.2016.11.012.

Simakov O*, Kawashima T*, Marlétaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, Bredeson J, Shoguchi E, Gyoja F, Yue JX, Chen YC, Freeman RM Jr, Sasaki A, Hikosaka-Katayama T, Sato A, Fujie M, Baughman KW, Levine J, Gonzalez P, et al. Hemichordate genomes and deuterostome origins. Nature. 2015 Nov 26;527(7579):459-65. doi:10.1038/nature16150.

Baumgarten S, Simakov O, Esherick LY, Liew YJ, Lehnert EM, Michell CT, Li Y, Hambleton EA, Guse A, Oates ME, Gough J, Weis VM, Aranda M, Pringle JR, Voolstra CR. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc Natl Acad Sci USA. 2015 Sep 22;112(38):11893-8. doi:10.1073/pnas.1513318112.

Albertin CB*, Simakov O*, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature. 2015 Aug 13;524(7564):220-4. doi:10.1038/nature14668. (cover)

Petersen HO, Höger SK, Looso M, Lengfeld T, Kuhn A, Warnken U, Nishimiya-Fujisawa C, Schnölzer M, Krüger M, Özbek S, Simakov O, Holstein TW. A Comprehensive Transcriptomic and Proteomic Analysis of Hydra Head Regeneration. Mol Biol Evol. 2015 Aug;32(8):1928-47. doi:10.1093/molbev/msv079.

Simakov O, Marletaz F, Cho SJ, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo DH, Larsson T, Lv J, Arendt D, Savage R, Osoegawa K, de Jong P, Grimwood J, Chapman JA, Shapiro H, Aerts A, Otillar RP, Terry AY, Boore JL, et al. Insights into bilaterian evolution from three spiralian genomes. Nature. 2013 Jan 24;493(7433):526-31. doi:10.1038/nature11696.

Chapman JA*, Kirkness EF*, Simakov O*, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, et al. The dynamic genome of Hydra. Nature. 2010 Mar 25;464(7288):592-6. doi:10.1038/nature08830.

Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature. 2010 Aug 5;466(7307):720-6. doi:10.1038/nature09201.

Full publication list

(* Co-first or corresponding Author)

2019

Ritschard E, Whitelaw B, Albertin C, Cooke I, Strugnell J, Simakov O, Coupled genomic evolutionary histories as signatures of organismal innovations in cephalopods, BioEssays, in press 2019

Calcino AD, de Oliveira AL, Simakov O, Schwaha T, Zieger E, Wollesen T, Wanninger A, The quagga mussel genome and the evolution of freshwater tolerance, DNA Research, in press 2019, dsz019, doi.org/10.1093/dnares/dsz019

Zimmermann B, Robert NSM, Technau U, Simakov O*. Ancient animal genome architecture reflects cell type identities. Nat Ecol Evol. 2019 Aug 5. doi: 10.1038/s41559-019-0946-7.

Zarrella I, Herten K, Maes GE, Tai S, Yang M, Seuntjens E, Ritschard EA, Zach M, Styfhals R, Sanges R, Simakov O*, Ponte G, Fiorito G*. The survey and reference assisted assembly of the Octopus vulgaris genome. Sci Data. 2019 Apr 1;6(1):13. doi: 10.1038/s41597-019-0017-6.

Ritschard EA*, Fitak RR, Simakov O*, Johnsen S. Genomic signatures of G-protein-coupled receptor expansions reveal functional transitions in the evolution of cephalopod signal transduction. Proc Biol Sci. 2019 Feb 27;286(1897):20182929. doi: 10.1098/rspb.2018.2929.

Styfhals R, Seuntjens E, Simakov O, Sanges R, Fiorito G. In silico Identification and Expression of Protocadherin Gene Family in Octopus vulgaris. Front Physiol. 2019 Jan 14;9:1905. doi: 10.3389/fphys.2018.01905.

Belcaid M, Casaburi G, McAnulty SJ, Schmidbaur H, Suria AM, Moriano-Gutierrez S, Pankey MS, Oakley TH, Kremer N, Koch EJ, Collins AJ, Nguyen H, Lek S, Goncharenko-Foster I, Minx P, Sodergren E, Weinstock G, Rokhsar DS, McFall-Ngai M, Simakov O*, Foster JS*, Nyholm SV*. Symbiotic organs shaped by distinct modes of genome evolution in cephalopods. Proc Natl Acad Sci USA. 2019 Feb 19;116(8):3030-3035. doi: 10.1073/pnas.1817322116. (cover)

2018

Wong WY, Simakov O*. RepeatCraft: a meta-pipeline for repetitive element de-fragmentation and annotation. Bioinformatics. 2018 Aug 25. doi: 10.1093/bioinformatics/bty745.

Revilla-I-Domingo R, Simakov O*. The Diversification of Early Emerging Metazoans: A Window into the Evolution of Animal Multicellularity. Bioessays.2018 May;40(5):e1800029. doi:10.1002/bies.201800029.

Sanchez G, Setiamarga DHE, Tuanapaya S, Tongtherm K, Winkelmann IE, Schmidbaur H, Umino T, Albertin C, Allcock L, Perales-Raya C, Gleadall I, Strugnell JM, Simakov O*, Nabhitabhata J*. Genus-level phylogeny of cephalopods using molecular markers: current status and problematic areas. PeerJ. 2018 Feb 12;6:e4331. doi: 10.7717/peerj.4331.

2017

Simakov O*, Kawashima T. Independent evolution of genomic characters during major metazoan transitions. Dev Biol. 2017 Jul 15;427(2):179-192. doi: 10.1016/j.ydbio.2016.11.012.

2016

Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep. 2016 Dec 22;6:39734. doi: 10.1038/srep39734.

Session AM, Uno Y, Kwon T, Chapman JA, Toyoda A, Takahashi S, Fukui A, Hikosaka A, Suzuki A, Kondo M, van Heeringen SJ, Quigley I, Heinz S, Ogino H, Ochi H, Hellsten U, Lyons JB, Simakov O, Putnam N, Stites J, et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature. 2016 Oct 20;538(7625):336-343. doi:10.1038/nature19840.

Levin M, Anavy L, Cole AG, Winter E, Mostov N, Khair S, Senderovich N, Kovalev E, Silver DH, Feder M, Fernandez-Valverde SL, Nakanishi N, Simmons D, Simakov O, Larsson T, Liu SY, Jerafi-Vider A, Yaniv K, Ryan JF, Martindale MQ, et al. The mid-developmental transition and the evolution of animal body plans. Nature. 2016 Mar 31;531(7596):637-641. doi: 10.1038/nature16994.

2015

Simakov O*, Kawashima T*, Marlétaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, Bredeson J, Shoguchi E, Gyoja F, Yue JX, Chen YC, Freeman RM Jr, Sasaki A, Hikosaka-Katayama T, Sato A, Fujie M, Baughman KW, Levine J, Gonzalez P, et al. Hemichordate genomes and deuterostome origins. Nature. 2015 Nov 26;527(7579):459-65. doi: 10.1038/nature16150.

Ramanathan N*, Simakov O*, Merten CA, Arendt D. Quantifying Preferences and Responsiveness of Marine Zooplankton to Changing Environmental Conditions using Microfluidics. PLoS One. 2015 Oct 30;10(10):e0140553. doi:10.1371/journal.pone.0140553.

Baumgarten S, Simakov O, Esherick LY, Liew YJ, Lehnert EM, Michell CT, Li Y, Hambleton EA, Guse A, Oates ME, Gough J, Weis VM, Aranda M, Pringle JR, Voolstra CR. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc Natl Acad Sci USA. 2015 Sep 22;112(38):11893-8. doi: 10.1073/pnas.1513318112.

Albertin CB*, Simakov O*, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature. 2015 Aug 13;524(7564):220-4. doi: 10.1038/nature14668. (cover)

Wäge J, Hardege JD, Larsson TA, Simakov O, Chapman EC, Arendt D, Rotchell JM. Effects of low seawater pH on the marine polychaete Platynereis dumerilii. Mar Pollut Bull. 2015 Jun 15;95(1):166-72. doi: 10.1016/j.marpolbul.2015.04.027.

Petersen HO, Höger SK, Looso M, Lengfeld T, Kuhn A, Warnken U, Nishimiya-Fujisawa C, Schnölzer M, Krüger M, Özbek S, Simakov O, Holstein TW. A Comprehensive Transcriptomic and Proteomic Analysis of Hydra Head Regeneration. Mol Biol Evol. 2015 Aug;32(8):1928-47. doi: 10.1093/molbev/msv079.

2014

Lauri A, Brunet T, Handberg-Thorsager M, Fischer AH, Simakov O, Steinmetz PR, Tomer R, Keller PJ, Arendt D. Development of the annelid axochord: insights into notochord evolution. Science. 2014 Sep 12;345(6202):1365-8. doi: 10.1126/science.1253396.

Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S, Simakov O, Ng AY, Lim ZW, Bezault E, Turner-Maier J, Johnson J, Alcazar R, Noh HJ, Russell P, Aken B, Alföldi J, Amemiya C, Azzouzi N, Baroiller JF, et al. Nature. 2014 Sep 18;513(7518):375-381. doi:10.1038/nature13726.

Chalopin D, Fan S, Simakov O, Meyer A, Schartl M, Volff JN. Evolutionary active transposable elements in the genome of the coelacanth. J Exp Zool B Mol Dev Evol. 2014 Sep;322(6):322-33. doi: 10.1002/jez.b.22521.

2013

Amemiya CT, Alföldi J, Lee AP, Fan S, Philippe H, Maccallum I, Braasch I, Manousaki T, Schneider I, Rohner N, Organ C, Chalopin D, Smith JJ, Robinson M, Dorrington RA, Gerdol M, Aken B, Biscotti MA, Barucca M, Baurain D,et al. The African coelacanth genome provides insights into tetrapod evolution. Nature. 2013 Apr 18;496(7445):311-6. doi:10.1038/nature12027. (cover)

Simakov O, Marletaz F, Cho SJ, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo DH, Larsson T, Lv J, Arendt D, Savage R, Osoegawa K, de Jong P, Grimwood J, Chapman JA, Shapiro H, Aerts A, Otillar RP, Terry AY, Boore JL, et al. Insights into bilaterian evolution from three spiralian genomes. Nature. 2013 Jan 24;493(7433):526-31. doi: 10.1038/nature11696.

Simakov O, Larsson TA, Arendt D. Linking micro- and macro-evolution at the cell type level: a view from the lophotrochozoan Platynereis dumerilii. Brief Funct Genomics. 2013 Sep;12(5):430-9. doi: 10.1093/bfgp/els049.

2010

Gurley KA, Elliott SA, Simakov O, Schmidt HA, Holstein TW, Sánchez Alvarado A. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev Biol. 2010 Nov 1;347(1):24-39. doi: 10.1016/j.ydbio.2010.08.007.

Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature. 2010 Aug 5;466(7307):720-6. doi: 10.1038/nature09201.

Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, et al. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science. 2010 Jul 9;329(5988):223-6. doi: 10.1126/science.1188800.

Chapman JA*, Kirkness EF*, Simakov O*, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, et al. The dynamic genome of Hydra. Nature. 2010 Mar 25;464(7288):592-6. doi:10.1038/nature08830.

Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K, Klaus S, Snyman H, Hannon GJ, Bork P, Arendt D. Ancient animal microRNAs and the evolution of tissue identity. Nature. 2010 Feb 25;463(7284):1084-8. doi: 10.1038/nature08744.

2009

Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Ozbek S, Bode H, Holstein TW. Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol. 2009 Jun 1;330(1):186-99. doi:10.1016/j.ydbio.2009.02.004.

2006

Melcher C, Bader R, Walther S, Simakov O, Pankratz MJ. Neuromedin U and its putative Drosophila homolog hugin. PLoS Biol. 2006 Mar;4(3):e68. PubMed PMID: 16524341; PubMed Central PMCID: PMC1397894.