Publications

Hehenberger, E. and Burki, F. (2024) The Extent, Role, and Timing of Endosymbiotic Gene Transfer in Plastids. In: Schwartzbach, S. D., Kroth, P. G., Oborník, M. (eds) Endosymbiotic Organelle Acquisition. Springer, Cham. doi: https://doi.org/10.1007/978-3-031-57446-7_4

Cooney, E. C., Holt, C. C., Hehenberger, E., Adams, J. A., Leander, B. S., and Keeling, P. J. (2024) Investigation of heterotrophs reveals new insights in dinoflagellate evolution. Mol. Phylogenet. Evol. 196, 108086. doi: https://doi.org/10.1016/j.ympev.2024.108086

del Campo, J., Carlos-Oliveira, M., Čepička, I., Hehenberger, E., Horák, A., Karnkowska, A., Kolisko, M., Lara, E., Lukeš, J., Pánek, T., Piwosz, K., Richter, D. J., Škaloud, P., Sutak, R., Tachezy, J. & Hampl, V. The protist cultural renaissance. Trends Microbiol. (2023). doi: https://doi.org/10.1016/j.tim.2023.11.010

Harbeitner, R. C., Wittmers, F., Yung, C. C. M., Eckmann, C. A., Hehenberger, E., Blum, M., Needham, D. M. and Worden, A. Z. (2024) Gradients of bacteria in the oceanic water column reveal finely-resolved vertical distributions. PLOS ONE 19(4): e0298139. doi: https://doi.org/10.1371/journal.pone.0298139

Hehenberger, E., Guo, J., Wilken, S., Hoadley, K., Sudek, L., Poirier, C., Dannebaum, R., Susko, E. & Worden, A. Z. Phosphate limitation responses in marine green algae are linked to reprogramming of the tRNA epitranscriptome and codon usage bias. Mol. Biol. Evol. msad251 (2023). doi: https://doi.org/10.1093/molbev/msad251

Holt, C. C.*, Hehenberger, E.*, Tikhonenkov, D. V., Jacko-Reynolds, V. K. L., Okamoto, N., Cooney, E. C., Irwin, N. A. T. & Keeling, P. J. Multiple parallel origins of parasitic Marine Alveolates. Nat. Commun. 14, (2023). doi: https://doi.org/10.1038/s41467-023-42807-0
* These authors contributed equally

Hehenberger, E., Boscaro, V., James, E. R., Hirakawa, Y., Trznadel, M., Mtawali, M., Fiorito, R., del Campo, J., Karnkowska, A., Kolisko, M., Irwin, N. A. T., Mathur, V., Scheffrahn, R. H. & Keeling, P. J. New Parabasalia symbionts Snyderella spp. and Daimonympha gen. nov. from South American Rugitermes termites and the parallel evolution of a cell with a rotating “head”. J. Eukaryot. Microbiol. 70, e12987 (2023).

Decelle, J., Kayal, E., Bigeard, E., Gallet, B., Bougoure, J., Clode, P., Schieber, N., Templin, R., Hehenberger, E., Prensier, G., Chevalier, F., Schwab, Y. & Guillou, L. Intracellular development and impact of a marine eukaryotic parasite on its zombified microalgal host. ISME J. 16, 2348–2359 (2022).

Cho, A., Tikhonenkov, D. V, Hehenberger, E., Karnkowska, A., Mylnikov, A. P. & Keeling, P. J. Monophyly of diverse Bigyromonadea and their impact on phylogenomic relationships within stramenopiles. Mol. Phylogenet. Evol. 171, 107468 (2022).

Wittmers, F., Needham, D. M., Hehenberger, E., Giovannoni, S. J. & Worden, A. Z. Genomes from uncultivated pelagiphages reveal multiple phylogenetic clades exhibiting extensive auxiliary metabolic genes and cross-family multigene transfers. mSystems 7, e01522-21 (2022).

Bachy, C., Hehenberger, E., Ling, Y.-C., Needham, D. M., Strauss, J., Wilken, S. & Worden, A. Z. in (eds. Stal, L. J. & Cretoiu, M. S.) 159–241 (Springer International Publishing, 2022). doi:https://doi.org/10.1007/978-3-030-90383-1_4

Hamilton, M., Mascioni, M., Hehenberger, E., Bachy, C., Yung, C., Vernet, M. & Worden, A. Z. Spatiotemporal variations in Antarctic protistan communities highlight phytoplankton diversity and seasonal dominance by a novel cryptophyte lineage. MBio 12, e02973-21 (2021).

Singh, R. A., Boscaro, V., James, E. R., Karnkowska, A., Kolisko, M., Gavelis, G. S., Okamoto, N., del Campo, J., Fiorito, R., Hehenberger, E., Irwin, N. A. T., Mathur, V., Scheffrahn, R. H. & Keeling, P. J. Characterization of new cristamonad species from kalotermitid termites including a novel genus, Runanympha. Sci. Rep. 11, 7270 (2021).

Hehenberger, E., Eitel, M., Fortunato, S. A. V., Miller, D. J., Keeling, P. J. & Cahill, M. A. Early eukaryotic origins and metazoan elaboration of MAPR family proteins. Mol. Phylogenet. Evol. 148, (2020).

Tikhonenkov, D. V.*, Mikhailov, K. V.*, Hehenberger, E., Karpov, S. A., Prokina, K. I., Esaulov, A. S., Belyakova, O. I., Mazei, Y. A., Mylnikov, A. P., Aleoshin, V. V & Keeling, P. J. New lineage of microbial predators adds complexity to reconstructing the evolutionary origin of animals. Curr. Biol. 30, 4500-4509.e5 (2020).
* These authors contributed equally

Tikhonenkov, D. V., Hehenberger, E., Esaulov, A. S., Belyakova, O. I., Mazei, Y. A., Mylnikov, A. P. & Keeling, P. J. Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals. BMC Biol. 18, 39 (2020).

Keeling, P. J., Boscaro, V., Bardell, F., Burki, F., Cho, A., Cooney, E. C., del Campo, J., Fast, N. M., Fiorito, R., Gavelis, G. S., Gawryluk, R. M. R., George, E. E., Gomm-Kolisko, R. N., Grisdale, C. J., Heger, T., Hehenberger, E., Herranz, M., Hirakawa, Y., Husnik, F., Imanian, B., Irwin, N. A. T., James, E. R., Janouskovec, J., Karnkowska, A., Kolisko, M., Kwong, W., Leander, B. S., Mathur, V., Nawar, F., Okamoto, N., Parfrey, L., Pittis, A., Pan, J., Pombert, J.-F., Sabetrasekh, M., Saldarriaga, J. F., Sanders, R., Singh, R. A., Smith, D. R., Strassert, J. F. H., Stephenson, I., Syberg-Olsen, M. J., Tai, V., Tikhonenkov, D. V, Van Steenkiste, N. W. L., Whalen, M., Whelan, T. A. & Wong, D. K. A letter to Denis Lynn. Aquat. Ecosyst. Health Manag. 23, 17–18 (2020).

Faktorová, D., Nisbet, R. E. R., Fernández Robledo, J. A., Casacuberta, E., Sudek, L., Allen, A. E., Ares, M., Aresté, C., Balestreri, C., Barbrook, A. C., Beardslee, P., Bender, S., Booth, D. S., Bouget, F. Y., Bowler, C., Breglia, S. A., Brownlee, C., Burger, G., Cerutti, H., Cesaroni, R., Chiurillo, M. A., Clemente, T., Coles, D. B., Collier, J. L., Cooney, E. C., Coyne, K., Docampo, R., Dupont, C. L., Edgcomb, V., Einarsson, E., Elustondo, P. A., Federici, F., Freire-Beneitez, V., Freyria, N. J., Fukuda, K., García, P. A., Girguis, P. R., Gomaa, F., Gornik, S. G., Guo, J., Hampl, V., Hanawa, Y., Haro-Contreras, E. R., Hehenberger, E., Highfield, A., Hirakawa, Y., Hopes, A., Howe, C. J., Hu, I., Ibañez, J., Irwin, N. A. T., Ishii, Y., Janowicz, N. E., Jones, A. C., Kachale, A., Fujimura-Kamada, K., Kaur, B., Kaye, J. Z., Kazana, E., Keeling, P. J., King, N., Klobutcher, L. A., Lander, N., Lassadi, I., Li, Z., Lin, S., Lozano, J. C., Luan, F., Maruyama, S., Matute, T., Miceli, C., Minagawa, J., Moosburner, M., Najle, S. R., Nanjappa, D., Nimmo, I. C., Noble, L., Novák Vanclová, A. M. G., Nowacki, M., Nuñez, I., Pain, A., Piersanti, A., Pucciarelli, S., Pyrih, J., Rest, J. S., Rius, M., Robertson, D., Ruaud, A., Ruiz-Trillo, I., Sigg, M. A., Silver, P. A., Slamovits, C. H., Jason Smith, G., Sprecher, B. N., Stern, R., Swart, E. C., Tsaousis, A. D., Tsypin, L., Turkewitz, A., Turnšek, J., Valach, M., Vergé, V., von Dassow, P., von der Haar, T., Waller, R. F., Wang, L., Wen, X., Wheeler, G., Woods, A., Zhang, H., Mock, T., Worden, A. Z. & Lukeš, J. Genetic tool development in marine protists: emerging model organisms for experimental cell biology. Nat. Methods 17, 481–494 (2020).

Cooney, E. C., Okamoto, N., Cho, A., Hehenberger, E., Richards, T. A., Santoro, A. E., Worden, A. Z., Leander, B. S. & Keeling, P. J. Single-cell transcriptomics of Abedinium reveals a new early-branching dinoflagellate lineage. Genome Biol. Evol. 12, 2417–2428 (2020).

Mathur, V.*, Kolísko, M.*, Hehenberger, E., Irwin, N. A. T., Leander, B. S., Kristmundsson, Á., Freeman, M. A. & Keeling, P. J. Multiple independent origins of apicomplexan-like parasites. Curr. Biol. 29, 2936-2941.e5 (2019).
* These authors contributed equally

Gawryluk, R. M. R.*, Tikhonenkov, D. V.*, Hehenberger, E., Husnik, F., Mylnikov, A. P. & Keeling, P. J. Non-photosynthetic predators are sister to red algae. Nature 572, 240–243 (2019).
* These authors contributed equally

Needham, D. M., Poirier, C., Hehenberger, E., Jiménez, V., Swalwell, J. E., Santoro, A. E. & Worden, A. Z. Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes. Philos. Trans. R. Soc. B Biol. Sci. 374, 20190086 (2019).

Irwin, N. A. T., Tikhonenkov, D. V, Hehenberger, E., Mylnikov, A. P., Burki, F. & Keeling, P. J. Phylogenomics supports the monophyly of the Cercozoa. Mol. Phylogenet. Evol. 130, 416–423 (2019).

Strassert, J. F. H., Hehenberger, E., del Campo, J., Okamoto, N., Kolisko, M., Richards, T. A., Worden, A. Z., Santoro, A. E. & Keeling, P. J. Phylogeny, evidence for a cryptic plastid, and distribution of Chytriodinium parasites (Dinophyceae) infecting copepods. J. Eukaryot. Microbiol. 66, 574–581 (2019).

Needham, D. M.*, Yoshizawa, S.*, Hosaka, T.*, Poirier, C., Choi, C. J., Hehenberger, E., Irwin, N. A. T., Wilken, S., Yung, C.-M., Bachy, C., Kurihara, R., Nakajima, Y., Kojima, K., Kimura-Someya, T., Leonard, G., Malmstrom, R. R., Mende, D. R., Olson, D. K., Sudo, Y., Sudek, S., Richards, T. A., DeLong, E. F., Keeling, P. J., Santoro, A. E., Shirouzu, M., Iwasaki, W. & Worden, A. Z. A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. Proc. Natl. Acad. Sci. 116, 20574–20583 (2019).
* These authors contributed equally

Hehenberger, E., Gast, R. J. & Keeling, P. J. A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Proc. Natl. Acad. Sci. U. S. A. 116, 17934–17942 (2019).

Strassert, J. F. H., Karnkowska, A., Hehenberger, E., Del Campo, J., Kolisko, M., Okamoto, N., Burki, F., Janouškovec, J., Poirier, C., Leonard, G., Hallam, S. J., Richards, T. A., Worden, A. Z., Santoro, A. E. & Keeling, P. J. Single cell genomics of uncultured marine alveolates shows paraphyly of basal dinoflagellates. ISME J. 12, 304–308 (2018).

Hehenberger, E., James, E. R., del Campo, J., Buckland-Nicks, J. A., Reimchen, T. E. & Keeling, P. J. Fish parasite dinoflagellates Haidadinium ichthyophilum and Piscinoodinium share a recent common ancestor. J. Eukaryot. Microbiol. 65, 127–131 (2018).

Boscaro, V., James, E. R., Fiorito, R., Hehenberger, E., Karnkowska, A., del Campo, J., Kolisko, M., Irwin, N. A. T., Mathur, V., Scheffrahn, R. H. & Keeling, P. J. Molecular characterization and phylogeny of four new species of the genus Trichonympha (Parabasalia, Trichonymphea) from lower termite hindguts. Int. J. Syst. Evol. Microbiol. 67, 3570–3575 (2017).

Hehenberger, E., Tikhonenkov, D. V, Kolisko, M., del Campo, J., Esaulov, A. S., Mylnikov, A. P. & Keeling, P. J. Novel predators reshape holozoan phylogeny and reveal the presence of a two-component signaling system in the ancestor of animals. Curr. Biol. 27, 2043-2050.e6 (2017).

del Campo, J., James, E. R., Hirakawa, Y., Fiorito, R., Kolisko, M., Irwin, N. A. T., Mathur, V., Boscaro, V., Hehenberger, E., Karnkowska, A., Scheffrahn, R. H. & Keeling, P. J. Pseudotrichonympha leei, Pseudotrichonympha lifesoni, and Pseudotrichonympha pearti, new species of parabasalian flagellates and the description of a rotating subcellular structure. Sci. Rep. 7, 16349 (2017).

del Campo, J., Guillou, L., Hehenberger, E., Logares, R., López-García, P. & Massana, R. Ecological and evolutionary significance of novel protist lineages. Eur. J. Protistol. 55, 4–11 (2016).

Hehenberger, E., Burki, F., Kolisko, M. & Keeling, P. J. Functional relationship between a dinoflagellate host and its diatom endosymbiont. Mol. Biol. Evol. 33, 2376–2390 (2016).

Hehenberger, E., Imanian, B., Burki, F. & Keeling, P. J. Evidence for the retention of two evolutionary distinct plastids in dinoflagellates with diatom endosymbionts. Genome Biol. Evol. 6, 2321–2334 (2014).

Burki, F.*, Imanian, B.*, Hehenberger, E., Hirakawa, Y., Maruyama, S. & Keeling, P. J. Endosymbiotic gene transfer in tertiary plastid-containing dinoflagellates. Eukaryot. Cell 13, 246–255 (2014).
* These authors contributed equally

Probst, O. C., Karayel, E., Schida, N., Nimmerfall, E., Hehenberger, E., Puxbaum, V. & Mach, L. The mannose 6-phosphate-binding sites of M6P/IGF2R determine its capacity to suppress matrix invasion by squamous cell carcinoma cells. Biochem. J. 451, 91–99 (2013).

Hehenberger, E., Kradolfer, D. & Köhler, C. Endosperm cellularization defines an important developmental transition for embryo development. Development 139, 2031–2039 (2012).

Weinhofer, I., Hehenberger, E., Roszak, P., Hennig, L. & Köhler, C. H3K27me3 profiling of the endosperm implies exclusion of Polycomb Group Protein targeting by DNA methylation. PLOS Genet. 6, e1001152 (2010).