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

Simakov, O. and T. Kawashima. "Independent evolution of genomic characters during major metazoan transitions." Dev Biol, 2016

 

Simakov O*, Kawashima T*, Marletaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, et al. (2015). “Hemichordate genomes and deuterostome origins.” Nature 527(7579):459-65 [*, equal contributions]

 

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 U S A. 2015 Sep 22;112(38):11893-8.

 

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.

 

Albertin CB*, Simakov O*, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS. (2015) “The octopus genome and the evolution of cephalopod neural and morphological novelties.” Nature 524(7564):220-4. [*, equal contributions]

 

Simakov O, Marletaz F, Cho SJ, Edsinger-Gonzales E, et al. (2013). “Insights into bilaterian evolution from three spiralian genomes” Nature. 493(7433):526-31.

 

Chapman JA*, Kirkness EF*, Simakov O*, et al. (2010). “The dynamic genome of Hydra.” Nature 464(7288):592-6. [*, equal contributions]

 

Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, et al. (2010). “The Amphimedon queenslandica genome and the evolution of animal complexity.” Nature 466(7307):720-6

 

 

Full publication list

(* Co-first or corresponding Author)

2019

  • Zarrella I, Herten K, Maes G, Tai S, Yang M, Seuntjens E, Ritschard E, 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 in press

  • Ritschard E, Fitak R, Simakov O*, Johnsen S.  Genomic signatures of GPCR expansions reveal functional transitions in the evolution of cephalopod signal transduction. Proc Biol Sci., 2019, in press

  • 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. eCollection 2018.

  • Belcaid M, G Casaburi, SJ McAnulty, H Schmidbaur, AM Suria, S Moriano-Gutierrez, MS Pankey, TH Oakley, N Kremer , EJ Koch, AJ Collins, H Nguyen, S Lek, Irina Goncharenko, P Minx, E Sodergren, G Weinstock, D Rokhsar, M McFall-Ngai, O Simakov*, JS Foster*, SV Nyholm* “Symbiotic organs shaped by distinct modes of genome evolution in cephalopods.” Proc Natl Acad Sci U S A. 2019 (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. Epub 2018 Mar 25. PubMed PMID: 29575018.
  • 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*. (2018) Genus-level phylogeny of cephalopods using molecular markers: current status and problematic areas. PeerJ 6:e4331 

 2017

  • Simakov, O. and T. Kawashima. "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

  • Levin, M., L. Anavy, A. G. Cole, E. Winter, N. Mostov, S. Khair, N. Senderovich, E. Kovalev, D. H. Silver, M. Feder, S. L. Fernandez-Valverde, N. Nakanishi, D. Simmons, O. Simakov, T. Larsson, S.-Y. Liu, A. Jerafi-Vider, K. Yaniv, J. F. Ryan, M. Q. Martindale, J. C. Rink, D. Arendt, S. M. Degnan, B. M. Degnan, T. Hashimshony and I. Yanai. "The mid-developmental transition and the evolution of animal body plans."Nature, 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
  • Session, A. M., Y. Uno, T. Kwon, J. A. Chapman, A. Toyoda, S. Takahashi, et al. "Genome evolution in the allotetraploid frog Xenopus laevis." Nature, 2016.

2015

  • Simakov O*, Kawashima T*, Marletaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, et al. (2015). “Hemichordate genomes and deuterostome origins.” Nature 527(7579):459-65
  • 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 U S A. 2015 Sep 22;112(38):11893-8.
  • Albertin CB*, Simakov O*, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS. (2015) “The octopus genome and the evolution of cephalopod neural and morphological novelties.” Nature 524(7564):220-4.
  • 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.
  • Wäge, J., Hardege, J.D., Larsson, T.A., Simakov, O., Chapman, E.C., Arendt, D. and Rotchell, J.M. Effects of low seawater pH on the marine polychaete Platynereis dumerilii. Mar pol bul 2015, 95(1), pp.166-172
  • 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.

2014

  • Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S, Simakov O, et al. The genomic substrate for adaptive radiation in African cichlid fish. Nature. 2014 Sep 18;513(7518):375-81.
  • 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
  • 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.

2013

  • Simakov O, Marletaz F, Cho SJ, Edsinger-Gonzales E, et al. (2013). “Insights into bilaterian evolution from three spiralian genomes” Nature. 493(7433):526-31. 
  • Amemiya CT, Alföldi J, Lee AP, Fan S, Philippe H, et al. (2013) “The African coelacanth genome provides insights into tetrapod evolution.” Nature 496(7445):3

 2012

  • Simakov O, Larsson TA, Arendt D (2012).  “Linking micro- and macro-evolution at the cell type level: a view from the lophotrochozoan Platynereis dumerilii.” Brief Funct Genomics 20 Nov 2012 

2010

  • Chapman JA*, Kirkness EF*, Simakov O*, et al. (2010). “The dynamic genome of Hydra.” Nature 464(7288):592-6.
  • Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, et al. (2010). “The Amphimedon queenslandica genome and the evolution of animal complexity.” Nature 466(7307):720-6.
  • Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, et al. (2010) “Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri.” Science 329(5988):223-6. 
  • Gurley KA, Elliott SA, Simakov O, Schmidt HA, Holstein TW, Sánchez Alvarado A (2010). “Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response.” Dev Biol. 347(1):24-39.
  • Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K, Klaus S, Snyman H, Hannon GJ, Bork P, Arendt D (2010). “Ancient animal microRNAs and the evolution of tissue identity.” Nature 463(7284):1084-8.

 2009

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

 2006

  • Melcher C, Bader R, Walther S, Simakov O, Pankratz MJ (2006).  “Neuromedin U and its putative Drosophila homolog hugin.” PLoS Biol 4(3):e68, 2006