FY2020 Annual Report

Evolutionary Genomics Unit
Assistant Professor Thomas Bourguignon

Back row, left to right:  Nobuaki Mizumoto, Menglin Wang, Yukihiro Kinjo, Kensei Kikuchi, Jigyasa Arora.

Middle row, left to right: Crystal Clitheroe, Esra Kaymak, Anna Prokhorova, Tracy Audicio, Simon Hellemans.

Front row, left to right: Tom Bourguignon, Ales Bucek.


This fiscal year was particularly challenging because of the COVID-19 pandemic. However, the impact of the pandemic on our work was relatively limited. During the financial year 2020, we kept on investigating the evolution of termites, cockroaches, and their associated microbes. We sequenced the DNA libraries of about 2000 termite samples and kept on working on the 50 termite genomes we started sequencing last year. We are currently processing these data and will publish them in the coming years. We also published a total of 20 peer-reviewed papers, including four papers in Nature index journals, and obtained three Kakenhi grants. 

1. Staff

  • Dr. Thomas Bourguignon, Assistant Professor
  • Dr. Ales Bucek, Postdoctoral Scholar
  • Dr. Lucia Zifcakova, Postdoctoral Scholar (Jun. 2017–May 2020)
  • Dr. Yukihiro Kinjo, Postdoctoral Scholar
  • Dr. Anna Prokhorova, Postdoctoral Scholar (Jan. 2021–)
  • Dr. Simon Hellemans, JSPS Fellow 
  • Dr. Nobuaki Mizumoto, JSPS Fellow (May. 2020–)
  • Crystal-Leigh Clitheroe, Research Unit Technician
  • Esra Kaymak, Research Unit Technician (Jan. 2021–)
  • Jigyasa Arora, Ph.D. Student
  • Menglin Wang, Ph.D. Student
  • Tracy Audicio, Ph.D. Student
  • Chihiro Arasaki, Research Unit Administrator

2. Collaborations

2.1 Historical biogeography of termites

  • Type of collaboration: Joint research
  • Researchers:
    • Professor Yves Roisin, University of Brussels
    • Professor Nathan Lo, University of Sydney
    • Professor Rudolf A. Scheffrahn, University of Florida
    • Professor Eliana Cancello, University of Sao Paulo
    • Professor Xiaodong Yang, Xishuangbanna Tropical Botanical Gargen
    • Associate Professor Jan Sobotnik, Czech University of Life Sciences
    • Associate Professor Theodore A. Evans, University of Western Australia
    • Associate Professor David Sillam-Dusses, University of Paris 13

2.2 Functional evolution of termite gut microbes

  • Type of collaboration: Joint research
  • Researchers:
    • Professor Andreas Brune, Max Planck Institute for Terrestrial Microbiology
    • Professor Nathan Lo, University of Sydney
    • Associate Professor Jan Sobotnik, Czech University of Life Sciences
    • Professor Gaku Tokuda, University of the Ryukyus

2.3 Functional evolution of termite genomes

  • Type of collaboration: Joint research
  • Researchers:
    • Associate Professor Dino McMahon, Free University of Berlin
    • Associate Professor Jan Sobotnik, Czech University of Life Sciences
    • Dr. Mark Harrison, University of Munster

3. Activities and Findings

3.1 Functional evolution of termite gut microbes

We are using the gut metagenomes of 221 termite samples to investigate the functional evolution of termite gut microbes. We selected termite species based on their diet and phylogenetic position to have a sampling representative of termite phylogenetic and ecological diversity. This dataset is the largest of its kind and allows us to investigate the functional evolution of the gut microbiome of an entire insect order. During the fiscal year 2020, we finished writing one paper and kept on processing the data

3.2 Evolution of genome size in the cockroach endosymbiont Blattabacterium and other prokaryotes

The evolutionary processes that drive variation in genome size across the tree of life remain unresolved. Effective population size (Ne) is thought to play an important role in shaping genome size, a key example being the reduced genomes of insect endosymbionts, which undergo population bottlenecks during transmission. However, the existence of reduced genomes in marine and terrestrial bacterial species with large Ne demand an alternative explanation. We analyzed the genomic variation among related strains of nine divergent phyla of prokaryotes, including Blattabacterium endosymbionts of cockroaches (Bacteroidetes) (Figure 1), Buchnera endosymbionts of aphids (Proteobacteria), and seven lineages of free-living prokaryotes. We found a strong link between mutation rate and genome reduction in most prokaryote lineages. In most cases, rates of gene loss strongly correlate with rates of both nonsynonymous (dN) and synonymous (dS) substitutions per site, but not their ratio (dN/dS), indicating that genome reduction is primarily associated with increased mutation rate, rather than changes in Ne, although the latter cannot be ruled out. Lineages with high dS and dN, as well as smaller genomes, lacked multiple DNA repair genes, providing a proximate cause for increased mutation rates. Our findings suggest that similar mechanisms drive genome reduction in both intracellular and free-living bacteria and enable a comprehensive theory of genome size evolution in prokaryotes. Our results have been published during the fiscal year 2020.

Figure 1: Maximum likelihood phylogenetic tree of Blattabacterium inferred from protein-coding genes shared among 67 sequenced strains. The 3rd codon sites were removed. Branch color indicated cumulative gene loss, and node symbols showed bootstrap support values. This tree is reproduced from our publication (Bourguignon et al. 2020).

3.3 Evolution of termite genomes

During the fiscal year 2019, we started sequencing about 50 termite genomes to investigate how termite genomes have evolved over the last 150 million years. We are sequencing these genomes using a combination of sequencing approaches, including long reads generated with the promethION platform, short reads for polishing generated with the Illumina platform, and linked reads obtained with the Omni-C technology and sequenced on the Illumina platform. We carried out further sequencing during the fiscal year 2020 and started developing the bioinformatics pipeline we will use for this project. During the FY2021, we will do the last sequencing runs and analyze the genomes in a comparative genomics framework.

4. Publications

4.1 Journals

  1. William, K. A., Clitheroe, C-L., Villet, M. H., Midgley, J. M., The first record of Omosita nearctica Kirejtshuk (Coleoptera, Nitidulidae) in South Africa, with the first description of its mature larva. African Invertebrates, Vol. 62(1), pp. 257-271, doi: 10.3897/AfrInvertebr.62.58842 (2021)
  2. Jambor, H., Antonietti, A., Alicea, B. J., Audisio, T. L., ..., Weissgerber, T. L. Creating clear and informative image-based figures for scientific publications. PLOS Biology, Vol. 19(3), pp. e3001161, doi: 10.1371/journal.pbio.3001161 (2021)
  3. Chouvenc, T., Šobotník, J., Engel, M.S. & Bourguignon, T. Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cellular and Molecular Life Science, Vol. 78, pp. 2749-2769, doi: 10.1007/s00018-020-03728-z (2021)
  4. Soukup, P., Vetrovsky, T., Stiblik, P., Votypkova, K., Chakraborty, A., Sillam-Dussès, D., Kolarik, M., Odriozola, I., Lo, N., Baldrian, P., Šobotník, J. & Bourguignon, T. Termites are associated with external species-specific bacterial communities. Applied and Environmental Microbiology, Vol. 87(2), pp. e2042-20, doi: 10.1128/AEM.02042-20 (2021)
  5. Sillam-Dussès, D., Hradecky, J., Stiblik, P., Ferreira da Cunha, H., Carrijo, T.F., Lacey, M.J., Bourguignon, T. & Šobotník, J. The trail-following pheromone of the termite Serritermes serriferChemoecology, Vol. 31, pp. 11-17, doi: 10.1007/s00049-020-00324-2 (2020)
  6. Vetrovsky, T., Soukup, P., Stiblik, P., Votypkova, K., Chakraborty, A., Odriozola, I., Sillam-Dussès, D., Lo, N., Bourguignon, T., Baldrian, P., Šobotník, J. & Kolarik, M. Termites host specific fungal communities that differ from those in their ambient environments. Fungal Ecology Vol. 48, pp. 100991, doi: 10.1016/j.funeco.2020.100991 (2020)
  7. Le Lay, C. Le., Shi, M., Buček A., Bourguignon, T., Lo, N. Holmes EC. Unmapped RNA virus diversity in termites and their symbionts. Viruses, Vol. 12(10), pp. 1145, doi: https://doi.org/10.3390/v12101145 (2020)
  8. Buček, A., Vazdar, M., Tupec, M., Svatoš, A., Pichová, I. Desaturase specificity is controlled by the physicochemical properties of a single amino acid residue in the substrate binding tunnel. Comput Struct Biotechnol Journal, Vol. 18, pp. 1202–1209, doi: https://doi.org/10.1016/j.csbj.2020.05.011 (2020)
  9. Villa-Martín, P., Buček, A., Bourguignon, T., Pigolotti, S. Ocean currents promote rare species diversity in protists. Science Advances, Vol. 6(29), eaaz9037, doi: https://doi.org/10.1126/sciadv.aaz9037 (2020)
  10. Bourguignon, T., Kinjo, Y., Villa-Martin, P., Coleman, N. V., Tang, Q., Arab, D. A., Wang, Z., Tokuda, G., Hongoh, Y., Ohkuma, M., Pigolotti, S., Lo, N. Increased mutation rate is linked to genome reduction in prokaryotes. Current Biology, Vol. 30(19), pp. 3848-3855, doi: https://doi.org/10.1016/j.cub.2020.07.034 (2020)
  11. Hellemans, S., Deligne, J., Roisin, Y., Josens, G. Phylogeny and revision of the ‘Cubitermes complex’ termites (Termitidae: Cubitermitinae). Systematic Entomology, Vol. 46(1), pp. 224-238, doi: 10.1111/syen.12458 (2020)
  12. Hellemans, S., Roisin, Y. Asexual queen succession in termites. eLS, Vol. 1(1), doi: https://doi.org/10.1002/9780470015902.a0029115 (2020)
  13. Couto, A. A. V. D. O., Hellemans, S., Roisin, Y., Montes, M. A., Vasconcellos, A. Effects of habitat loss on the genetic diversity of Embiratermes neotenicus (Isoptera) in a fragmented landscape of Atlantic forest, Brazil. Insect Conservation and Diversity, Vol. 13(4), pp. 351-359, doi: 10.1111/icad.12414 (2020)
  14. Taerum, S., Jasso-Selles, D. E., Hileman, J., De Martini, F., Mizumoto, N., Gile, G. H. Spirotrichonymphea (Parabasalia) symbionts of the termite Paraneotermes simplicicornisEuropean Journal of Protistology, Vol. 76, pp. 125742, doi: 10.1016/j.ejop.2020.125742 (2020)
  15. Mizumoto, N., Rizo, A., Pratt, S.C. & Chouvenc, T. Termite males enhance mating encounters by changing speed according to density. Journal of Animal Ecology, Vol. 89(11), pp. 2542-2552, doi: 10.1111/1365-2656.13320 (2020)
  16. Valentini, G., Mizumoto, N., Pratt, S.C., Pavlic, T.P., Walker, S.I. Revealing the structure of information flows discriminates similar animal social behaviors. eLife, Vol. 9, pp. e55395, doi:10.7554/eLife.55395 (2020)
  17. Sillam-Dussès, D., Šobotník, J., Bourguignon, T., Wen, P., Semon, E., Robert, A., Cancello, E.M., Leroy, C., Lacey, M.J. & Bordereau, C. Trail-following pheromones in the termite subfamily Syntermitinae (Blattodea, Termitodae, Termitidae). Journal of Chemical Ecology, Vol. 46(5-6), pp. 475-482, doi: 10.1007/s10886-020-01180-8 (2020)
  18. Mizumoto, N., Gile, G. H. Pratt, S.C. Behavioral rules for soil excavation by colony founders and workers in termites. Annals of the Entomological Society of America, doi:10.1093/aesa/saaa017 (2020)
  19. Mizumoto, N., Bourguignon, T., Modern termites inherited the potential of collective construction from their common ancestor. Ecology and Evolution, Vol. 10(13) pp. 6775-6784, doi:10.1002/ece3.6381 (2020)
  20. Lowe E., Wolff J., Audisio T. L., …., Herberstein M. E. Towards establishment of a centralized spider traits database. Journal of Arachnology 48(2):103–109, doi: 10.1636/0161-8202-48.2.103 (2020)

4.2 Books and other one-time publications

  1. Bourguignon, T., Lo, N. Termite: phylogeny and classification. In: Starr C. (ed.) Encyclopedia of Social Insects. Springer Nature Switzerland AG. (2020)

4.3 Oral and Poster Presentations

  1. Lynch, C., Starkey, M., Mizumoto, N. A study on optimization sampling in multiple social insect colonies with a model-based approach, ABA 2020 Virtual Meeting, July 2020, (Oral)
  2. Mizumoto, N., Bardunias, P. M., Pratt, C. S. Complex relationship between tunneling patterns and individual behaviors in termites. The 22nd Annual Meeting of the Society of Evolutionary Studies, Japan, September2020, (Online, Poster Presentation)
  3. Mizumoto, N., 配偶者探索における雌雄の動きのパターンと遭遇率の研究, The 39th Annual Meeting of Japan Ethological Society, November 2020 (Online, Oral Presentation)
  4. Mizumoto, N., シロアリの建設行動と巣構造の関係, 令和2年度育志賞発表会, March 2021 (Online, Poster Presentation)
  5. Mizumoto, N., シロアリの集団行動の進化プロセス解明を目指して, 令和2年度育志賞発表会, March 2021, (Online, Oral Presentation)
  6. Mizumoto, N., Evolutionary perspectives of collective behavior, The 68th Annual Meeting of the Ecological Society of Japan, March 2021 (Online, Poster Presentation)
  7. Arora, J., Bourguignon T. 150 million years of evolution of gut microbiome in termites. Virtual Genomic Social Hour, California Academy of Sciences, June 2020 (Online Talk).
  8. Arora, J., Bourguignon T. Gut microbiome evolution across150 million years of termite evolution. Virtual Conference Microbiome, Cold Spring Harbor Laboratory, October 2020 (Online Talk).
  9. Bourguignon T. The genome evolution of Blattabacterium cuenoti, the endosymbiont of cockroaches. Seminar series of the Department of Entomology of the University of Georgia, USA. 8 February 2021 (Online Talk).

5. Intellectual Property Rights and Other Specific Achievements​

  • Grant-in-Aid for JSPS Fellows, Japan Society for the Promotion of Science, "Evolutionary process of termite construction revealed by comparative and constructive approaches", Lead PI: Mizumoto, N., Amount: 11.7M Yen, Period: April 2020–March 2023
  • Grant-in-Aid for Early-Career Scientists, Japan Society for the Promotion of Science, "Sustainable and efficient swine wastewater treatment with simultaneous removal of residual nitrates and nutrients recovery", Lead PI: Prokhorova, A., Amount: 3.51M Yen, Period: April 2020–March 2022
  • JSPS Fellows, Japan Society for the Promotion of Science, "Elucidating the evolutionary dynamics of the termite gut microbiome using shotgun metagenomics", Lead PI: Arora, J., Amount: 2M Yen, Period: April 2020–March 2022

6. Meetings and Events

6.1 シロアリの集団行動の進化プロセス解明を目指して

  • Date: September, 2020 (第69回つくば進化生態セミナー)
  • Venue: Online
  • Speaker: Dr. Nobuaki Mizumoto (OIST Evolutionary Genomics Unit)

7. Other

Nothing to report.