FY2019 Annual Report

Evolutionary Genomics Unit
Assistant Professor Thomas Bourguignon

(From left to right) Tracy Audicio, Tom Bourguignon, Simon Hellemans, Yukihiro Kinjo, Nobuaki Mizumoto, Menglin Wang, Jigyasa Arora and Crystal Clitheroe. Absent: Ales Bucek and Chihiro Arasaki.

Abstract

The Evolutionary Genomics Unit investigates the evolution and ecology of termites, cockroaches, and their associated microbes, using high-throughput sequencing methods. Our main research areas presently include: the evolution of symbiosis between insects and bacteria, the reconstruction of the insect tree of life, and the evolution of insect and bacterial genomes. During the fiscal year 2019, we sequenced 100s of termite and staphylinid mitochondrial genomes, and started sequencing about 30 termite genomes. We are currently processing these data, and we will publish them during the coming years.

1. Staff

  • Dr. Thomas Bourguignon, Assistant Professor
  • Dr. Ales Bucek, Postdoctoral Scholar
  • Dr. Lucia Zifcakova, Postdoctral Scholar
  • Dr. Taisuke Kanao, Postdoctoral Scholar
  • Dr. Yukihiro Kinjo, Postdoctoral Scholar
  • Dr. Simon Hellemans, JSPS Fellow (Nov. 2019 –) 
  • Dr. Shulin He, Visiting Researcher (Oct. 2019 – Mar. 2020)
  • Crystal-Leigh Clitheroe, Research Unit Technician
  • Jigyasa Arora, PhD Student
  • Menglin Wang, PhD Student
  • Tracy Audicio, PhD 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
    • 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 Evolution of cockroaches and their associated Blattabacterium

  • Type of collaboration: Joint research
  • Researchers:
    • Professor Gaku Tokuda, University of the Ryukyus
    • Professor Nathan Lo, University of Sydney
    • Associate Professor Simone Pigolotti, OIST

 

2.3 Evolution of termite genomes 

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

3. Activities and Findings

3.1 Evolution of termite symbiosis informed by transcriptome based phylogenies

Phylogenetic trees inferred using a handful of PCR-amplified markers often lack robustness, and sometime fail to resolve key nodes. The most robust termite phylogenetic trees have been produced from full mitochondrial genomes, which arguably is a single, albeit large, marker. To improve our understanding of termite natural history, we sequenced genomes and transcriptomes of 55 termite species, and built phylogenetic trees using up to 4065 orthologous genes of 68 species (Figure 1). Our phylogenetic trees were largely congruent with mitochondrial genome-based phylogenetic trees, but notably differ in the position of the bacterial comb-building Sphaerotermitinae that were unambiguously found to be the sister group of the fungus-growing Macrotermitinae. This branching pattern indicates that comb building is a derived trait within Termitidae, and therefore that the loss of cellulolytic gut protozoa might not have been caused by the creation of comb-like "external rumen" as previously hypothesized. 

Figure 1: Time-calibrated phylogenetic tree of termites inferred from manually-curated alignments of 462 orthologous genes, without third codon positions, using maximum likelihood inference. This tree is reproduced from our publication (Bucek et al. 2019).

3.2 Functional evolution of termite gut microbes

Termites harbor a large number of symbiotic microbes in their gut. Gut microbes provide their host with amino acids and vitamins and help digesting various types of organic matter, including wood, soil, and leaf litter. Few animal groups eat wood and soil, and how they evolved to do so is still largely unknown. We are using the gut metagenomes of 221 termite samples to investigate that question. This dataset represents the first attempt to elucidate the functional evolution of the gut microbiome of an insect order. During the fiscal year 2019, we kept on processing the data using the bioinformatics pipelines we developped, and started writing one paper. The analyses will continue during the next fiscal year.

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

Endosymbionts have reduced genomes that evolve in absence of gene input from outside sources. We studied the evolution of genome reduction in Blattabacterium, the endosymbiotic bacteria of cockroaches, with the aim of determining the factors that have led to gene loss in Blattabacterium since they were acquired by cockroaches about 220 million years ago. To our surprise, we found that the main factor leading to gene loss was mutation rate. We then investigated the link between gene loss and mutation rate in another eight lineages of bacteria and archaea and found that mutation rates strongly correlate with gene loss in six of them. Therefore, we found that mutation rate is a key driver of gene loss in prokaryotes. Our results have been accepted for publication, and the paper will be published during the course of the fiscal year 2020.

3.4 Evolution of termite genomes

To date, only a handful of termite genomes have been sequenced. Although these data are extremely valuable, they do not allow to investigate how termite genomes have been evolving since termite came to be 150 million years ago. To shed light on how termite genomes have evolved, we will sequence 50 termite genomes during the fiscal years 2019 and 2020. During the fiscal year 2019, we sequenced the genomes of 34 termite species using the promethION platform. We will carry out further sequencing during the coming fiscal year using a combination of platforms. 

4. Publications

4.1 Journals

  1. Arab, D.A., Bourguignon, T., Wang, Z., Ho, S.Y.W., Lo, N. Evolutionary rates are correlated between cockroach symbionts and mitochondrial genomes. Biology Letters, vol. 16, Issue 1, Page 2019702, doi: doi.org/10.1098/rsbl.2019.0702 (2020)
  2. Kanao, T., Iwata, R., Sasaki, T., Hirose, H. Yoshimura, M. New distributional records of two termitophilous rove beetles (Coleoptera, Staphylinidae) in Japan. Elytra New Series, vol. 9, No. 1, pp. 39–40, June 2019 (2019)
  3. Synek, J., Beránková, T., Stiblik, P., Pflegerová, J, Akama, P. D., Bourguignon, T., Sillam-Dussès, D., Šobotník, J., The oral gland, a new exocrine organ of termites, Arthropod Structure & Development, vol. 51, Pages 32-36, July 2019, doi: doi.org/10.1016/j.asd.2019.100876 (2019)
  4. Bucek, A., Šobotník, J., He, S., Shi, M., McMahon, D. P., Holmes, E. C., Roisin, Y., Lo, N., Bourguignon, T. Evolution of Termite Symbiosis Informed by Transcriptome-Based Phylogenies, Current Biology, vol. 29, Issue 21, Pages 3728-3734.e4, November 2019, doi: doi.org/10.1016/j.cub.2019.08.076 (2019)
  5. Forni, G., Puccio, G., Bourguignon, T., Evans, T., Mantovani, B., Rota-stabelli, O., Luchetti, A. Complete mitochondrial genomes from transcriptomes: assessing pros and cons of data mining for assembling new mitogenomes. Scientific Reports, vol. 9, Page 14806, October 2019, doi: 10.1038/s41598-019-51313-7 (2019)
  6. Delattre, O., Šobotník, J., Jandák, V., Synek, J., Cvačka, J., Jiřiček, O., Bourguignon, T., Sillam-Dussès, D. Chemical and vibratory signals used in alarm communication in the termite Reticulitermes flavipes (Rhinotermitidae). Insectes Sociaux, vol. 66, Issue 2, Pages 265-272, May 2019, doi: doi.org/10.1007/s00040-018-00682-9 (2019)
  7. Kanao, T., Maruyama, M. A new species of the termitophilous genus Trichopsenius Horn, 1877 (Coleoptera, Staphylinidae, Aleocharinae) from Morocco. Elytra New Series, vol. 9, No. 2, pp. 297–303, December 2019 (2019)

4.2 Books and other one-time publications

  1. Zifcakova, L. Factors affecting soil microbial processes. In Carbon and Nitrogen Cycling in Soil, R. Datta, R. S. Meena, S. I. Pathan, and M. T. Ceccherini, eds. (Singapore: Springer Singapore), pp. 439–461. doi: doi.org/10.1007/978-981-13-7264-3_13 (2020) 

4.3 Oral and Poster Presentations

  1. Wang, M., Bourguignon, T. Worldwide historical Biogeography of Termites (Blattodea: Isoptera). Termite Course 2019 in University of Florida, US. June, 2019 (2019)
  2. Arora, J., Zifcakova, L., Kinjo, Y., Bourguinon, T. Functional metagenomics and evolution of gut microbiome in termites. Association for Tropical Biology and Conservation (ATBC), Antananarivo, Madagascar, July 30 – August 3, 2019 (2019)
  3. Clitheroe C, Hellemans S, Roisin Y, Fournier D, Bourguignon T.  Genome sequence of Cavitermes tuberosus and its associated Wolbachia symbiont. Association for Tropical Biology and Conservation (ATBC), Antananarivo, Madagascar, July 30 – August 3, 2019 (2019)
  4. Bucek, A. et al. Evolution of digestive symbiotic systems in termites in the light of termite transcriptome phylogeny. Association for Tropical Biology and Conservation (ATBC), Antananarivo, Madagascar, July 30 – August 3, 2019 (2019)
  5. Audisio, T. L. Evolutionary ecology of the venom system in spiders. 21st Annual Meeting of the Japan Society for Evolutionary Studies, Hokkaido, Japan, August, 2019 (2019)
  6. Kinjo, Y., Bourguignon, T. 共生細菌のゲノム縮小進化を駆動する要因 (Driving factors of reductive genome evolution in endosymbionts). The 33th Annual Meeting of Japanese Society of Microbiral Ecology 2019, Yamanashi, Japan, September 11 – 13, 2019 (2019) 
  7. Bucek, A. Termites and food. Insect Experience Day (東京昆虫イベント「食とアートとサイエンス」), Tokyo, Japan, October 19, 2019 (2019)
  8. Arora, J. Unravelling 150 million years of evolution between termites and their gut microbiome using metagenomics. Mini-Symposium: Ecology and Evolution of Termite Gut microbes, OIST, Okinawa, Japan(2019)
  9. Zifcakova, L. Diet is the main factor affecting fungal gut microbiota of termites. Mini-Symposium: Ecology and Evolution of Termite Gut microbes, OIST, Okinawa, Japan (2019)
  10. Bourguignon, T. 150 millions years of coevolution between termites and their gut microbes. Mini-Symposium: Ecology and Evolution of Termite Gut microbes, OIST, Okinawa, Japan (2019)
  11. Kinjo, Y. Mutation-driven genome reduction in symbiotic bacteria. Mini-Symposium: Ecology and Evolution of Termite Gut microbes, OIST, Okinawa, Japan (2019)
  12. Bourguignon, T., Diet and cocladogenesis shape termite gut bacteria communities. The 13th conference of the Pacific-Rim Termite Research Group (PRTRG). Taipei, Taiwan. February 12 – 13, 2020 (2020)
  13. Hellemans, S., Marynowska, M., Drouet, T., Lepoint, G., Fournier, D., Calusinska, M., Roisin, Y., Characterizing the feeding behaviour of a generalist inquiline termite. The 13th conference of the Pacific-Rim Termite Research Group (PRTRG). Taipei, Taiwan. February 12 – 13, 2020 (2020)
  14. Bucek, A. et al. Evolution of Termite Symbiosis Informed by Transcriptome-Based Phylogenies. The 13th conference of the Pacific-Rim Termite Research Group (PRTRG), Taipei, Taiwan, February 12 – 13, 2020 (2020)
  15. Zifcakova, L., Clitheroe, C., Kinjo, Y., and Bourguignon, T., The Assembly of Fungal Communities in Termite Guts is Affected by Diet and Taxonomy. The 13th conference of the Pacific-Rim Termite Research Group (PRTRG), Taipei, Taiwan, February 12 – 13, 2020 (2020)
  16. Arora, J., Zifcakova, L., Kinjo, Y., Bourguinon, T.  Functional redundancy among gut bacteria of termites. Ecological Society of Japan (ESJ), Nagoya, Japan, March 4 – 8, 2020 (2020)
  17. Wang, M., Bourguignon, T. Worldwide historical Biogeography of Termites (Blattodea: Isoptera). 67th Annual Meeting of the Ecological Society of Japan, Aichi, Japan, March 4–8, 2020 (2020)
  18. Audisio, T. L. & Bourguignon, T. Evolutionary ecology of spiders obligate to termite nests. 67th Annual Meeting of the Ecological Society of Japan, Aichi, Japan, March 4 – 8, 2020 (2020)
  19. Zifcakova, L., Clitheroe, C., Kinjo, Y., and Bourguignon, T. Assembly of fungal communities in termite guts are driven by diet and location. 67th Annual Meeting of the Ecological Society of Japan, Aichi, Nagoya, March 4 – 8, 2020 (2020)

5. Intellectual Property Rights and Other Specific Achievements

  • Postdoctoral fellwship for foreign researchers, Japan Society for the Promotion of Science, "シロアリとその細胞内バクテリアの共生", Lead PI: Simon Hellemans, Amount: 10.38M Yen, Period: November 2019–October 2021
  • Grant-in-Aid for Yound Scientists, Japan Society for the Promotion of Science, "同種のシロアリを寄主とする好白蟻性昆虫の進化史の比較", Lead PI: Kanao, T., Amount: 4.16M Yen, Period: April 2019–March 2021
  • Grant-in-Aid for Yound Scientists, Japan Society for the Promotion of Science, "What is the molecular basis of parasitic manipulation in fly-termite system?", Lead PI: Bucek, A., Amount: 4.1M Yen, Period: April 2018–March 2020
  • Grant-in-Aid for Yound Scientists, Japan Society for the Promotion of Science, "Shedding light on genome evolution of a 220-million-year old's cockroach friend: Blattabacterium cuenoti", Lead PI: Bourguignon, T., Amount: 3.7M Yen, Period: April 2018–March 2020

6. Meetings and Events

6.1 Ecology and Evolution of Termite Gut Microbes

  • Date: December 1 – 4, 2019
  • Venue: Seminar Room C210, OIST Main Campus
  • Speaker: 
    • Aram Mikaelyan, North Carolina State University
    • Gillian Gile, Arizona State University
    • Andreas Brune, Max Planck Institute for Terrestrial Microbiology
    • Nathan Lo, The University of Sydney
    • Renate Radek, Free University of Berlin, Institute of Zoology
    • Yuichi Hongoh, Tokyo Institute of Technology
    • Moriya Ohkuma, RIKEN BioResource Research Center
    • Gaku Tokuda, University of the Ryukyus
    • Satoko Noda, University of Yamanashi
    • Wakako Ohtsubo, Tohoku University
    • Filip Husnik, University of British Columbia

7. Other

Nothing to report.