The phylum Heterolobosea Page and Blanton, 1985 is a group of eukaryotes that contains heterotrophic flagellates, amoebae, and amoeboflagellates, including the infamous brain-eating amoeba Naegleria fowleri. In this study, we investigate the deep evolutionary history of Heterolobosea by generating and analyzing transcriptome data from 16 diverse isolates and combine this with previously published data in a comprehensive phylogenomic analysis. This dataset has representation of all but one of the major lineages classified here as orders. Our phylogenomic analyses recovered a robustly supported phylogeny of Heterolobosea providing a phylogenetic framework for understanding their evolutionary history. Based on the newly recovered relationships, we revised the classification of Heterolobosea to the family level. We describe two new classes (Eutetramitea cl. nov. and Selenaionea cl. nov) and one new order (Naegleriida ord. nov.), and provide a new delimitation of the largest family of Heterolobosea, Vahlkampfiidae Jollos, 1917. Unexpectedly, we unveiled the first two cases of genetic code alterations in the group: UAG as a glutamine codon in the nuclear genome of Dactylomonas venusta and UGA encoding tryptophan in the mitochondrial genome of Neovahlkampfia damariscottae. In addition, analysis of the genome of the latter species confirmed its inability to make flagella, whereas we identified hallmark flagellum-specific genes in most other heteroloboseans not previously observed to form flagellates, suggesting that the loss of flagella in Heterolobosea is much rarer than generally thought. Finally, we define the first autapomorphy of the subphylum Pharyngomonada, represented by a fusion of two key genes for peroxisomal β-oxidation enzymes.

Charles University Faculty of Science Department of Zoology Prague Czechia

Dalhousie University Dept of Biochemistry and Molecular Biology Halifax Canada

Department of Biological Sciences Mississippi State University Mississippi State MS USA; Department of Biological Sciences Texas Tech University Lubbock TX USA

Department of Biological Sciences Mississippi State University Mississippi State MS USA; Institute for Genomics Biocomputing and Biotechnology Mississippi State University Mississippi State MS USA

Institute of Molecular Genetics Czech Academy of Sciences Prague Czech Republic Czechia

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czechia; University of Arkansas Department of Biological Sciences Fayetteville AR USA

Kyoto University Kyoto Japan

University of Ostrava Faculty of Science Department of Biology and Ecology Ostrava Czechia

University of Ostrava Faculty of Science Department of Biology and Ecology Ostrava Czechia; Department of Hematooncology Faculty of Medicine University of Ostrava Ostrava Czech Republic

University of Tsukuba Tsukuba Japan

University of Tsukuba Tsukuba Japan; Research Center for Advanced Analysis National Agriculture and Food Research Organization Tsukuba Ibaraki Japan

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