CRuMs
CRuMs is a clade of microbial eukaryotes proposed as a novel supergroup, named as an acronym for its three constituent lineages: Collodictyonidae (synonymous with Diphylleidae), Rigifilida, and Mantamonas.[1] These heterotrophic protists include free-swimming biflagellate collodictyonids such as Collodictyon triciliatum and Diphylleia rotans, the idiosyncratic filose amoeboflagellate Rigifila ramosa, and the gliding flagellate Mantamonas plastica.[1] In eukaryotic phylogenomics, CRuMs branches deeply as the sister group to Amorphea—the clade encompassing animals, fungi, and their amoeboid relatives—positioning it near the inferred root of the eukaryote tree of life.[1] This placement was robustly supported by analyses of up to 351 nuclear genes across diverse datasets using advanced site-heterogeneous mixture models.[1] The supergroup's discovery in 2018 resolved the orphan status of these lineages, previously unplaced in major eukaryotic assemblies, and highlighted their role in illuminating early eukaryotic diversification.[1] CRuMs members exhibit morphological diversity, from predatory flagellates with ventral feeding grooves to amoebae with rigid filopodia, reflecting adaptations to microbial food webs in aquatic and soil environments.[2] Recent genomic and transcriptomic studies have expanded the clade to include additional taxa, such as novel species like Glissandra oviformis, a predatory flagellate that underscores CRuMs' ecological significance as bacterivores and predators in protist communities.[2] Phylogenomic evidence consistently places CRuMs outside major supergroups like Diaphoretickes, Discoba, and Excavata, contributing to refined models of the eukaryote tree.[3] Ongoing research, including high-quality genomes from South Pacific isolates, reveals conserved traits like mitochondrial gene arrangements and protein complex retentions that distinguish CRuMs from other deep-branching eukaryotes.[4]Definition and History
Composition and Etymology
CRuMs is an acronym derived from its core constituent lineages: Collodictyonids (also known as Diphylleids), Rigifilids, and Mantamonads, representing a clade of heterotrophic microbial eukaryotes previously considered unrelated orphan groups in protist taxonomy.[1] The name was proposed in 2018 as a neutral, informal designation to unify these disparate lineages based on shared phylogenetic signals, avoiding taxonomic implications while highlighting their novel supergroup status.[1] The Collodictyonids comprise predatory flagellate protists bearing two or four flagella, characterized by a ventral feeding groove for phagocytosing prey, typically bacteria or smaller eukaryotes, and are found in freshwater and soil environments.[5] Rigifilids are filose amoeboflagellates with slender, rigid pseudopodia (filopodia) used for capturing bacterial prey, featuring a distinctive pellicle-supported body and occasional flagellar propulsion.[6] Mantamonads consist of small, gliding heterotrophic flagellates that move along substrates using a posterior flagellum, often in marine sediments, and exhibit a flattened, wing-like cell shape adapted for surface locomotion.[7] In 2025, the clade was expanded to include Glissandrida, a lineage of predatory biflagellate flagellates represented by species such as Glissandra oviformis, which exhibit gliding motility using subequal flagella emerging from a ventral depression and share ultrastructural features like a single-layered pellicle and lamellar mitochondrial cristae with other CRuMs members.[8] This addition, based on phylogenomic and morphological evidence, underscores the clade's growing diversity while maintaining the original acronym as a foundational term.[8]Discovery and Proposal
The historical recognition of CRuMs as a monophyletic clade in eukaryotic phylogeny arose from disparate morphological descriptions and molecular analyses of orphan protist lineages, gradually converging on their shared evolutionary history through the 20th and early 21st centuries. Initial observations focused on individual taxa without recognizing broader affinities. The genus Collodictyon, characterized by quadriflagellate cells with a ventral feeding groove, was first described from freshwater samples by H.J. Carter in 1865, marking one of the earliest records of a core CRuMs member.[9] Subsequent studies in the late 19th and early 20th centuries treated Collodictyon species as enigmatic heterotrophic flagellates, often classified loosely among sulcozoans or apusozoans due to their gliding motility and pseudopodial feeding, but lacking a unified phylogenetic context.[10] More recent discoveries in the 21st century illuminated additional lineages integral to CRuMs. The genus Mantamonas, comprising marine gliding zooflagellates with two heterodynamic flagella and a unique theca, was formally described by Glücksman et al. in 2011 from coastal sediments, initially positioned as a deep-branching apusozoan based on 18S rRNA gene sequences.[7] Shortly thereafter, in 2012, Yabuki, Ishida, and Cavalier-Smith described Rigifila ramosa, a filose protist with a rigid pellicle and branching filopodia, isolated from a freshwater paddy field in India; ultrastructural and SSU rRNA analyses placed it near micronuclearians, hinting at connections to other variosea-like forms.[11] These isolated studies highlighted the morphological diversity—ranging from biflagellate swimmers to filopodial amoeboflagellates—within what would emerge as CRuMs, but early molecular phylogenies often recovered them as unstable orphans near the base of the eukaryotic tree.[1] Preceding the formal establishment of CRuMs, provisional groupings attempted to accommodate these taxa amid evolving protist classifications. In 2013, Cavalier-Smith emended the infraphylum Varisulca to encompass mantamonads, collodictyonids (syn. diphylleids), and ancyromonads, based on shared cytological traits like ventral ciliary grooves and sulcal feeding mechanisms, positioning Varisulca as the basalmost podiate clade sister to Amorphea.[12] This framework provided an initial structural hypothesis but relied on limited multigene data and included Ancyromonas, whose placement later proved contentious. The definitive proposal of CRuMs as a novel supergroup-level clade came in 2018 from Brown et al., who conducted a phylogenomic analysis using 157–351 genes from 38 diverse eukaryotes, robustly uniting collodictyonids, rigifilids, and mantamonads with high bootstrap support (typically >90%) as the sister group to Amorphea within Opimoda; Ancyromonas was excluded, branching separately as a closer relative to Haptista.[1] This study marked a pivotal milestone by resolving long-unplaced lineages through genome-scale data, emphasizing CRuMs' early divergence in eukaryogenesis. In 2022, Zmitrovich, Perelygin, and Zharikov proposed elevating CRuMs to the kingdom Crumalia within their revised nine-kingdom eukaryotic system, incorporating it into subdomain Obimoda alongside Amorphea and Obazoa, based on integrated morphological and molecular syntheses.[13] However, this nomenclature was not broadly adopted, and subsequent phylogenomic works, including multigene analyses up to 2025, have reverted to the acronym CRuMs while affirming its monophyly and position adjacent to Amorphea.[14]Taxonomy
Classification Hierarchy
CRuMs is classified within the domain Eukaryota, where it occupies a deep-branching position robustly supported as the sister group to Amorphea (forming part of the broader Opimoda or Podiata assemblage) in phylogenomic studies.[1][2] The clade CRuMs itself lacks a formal phylum designation and is treated as an informal supergroup, consistent with the provisional and rank-flexible nature of protist taxonomy, which prioritizes monophyly over strict Linnaean ranks.[15] The clade was established by Brown et al. in 2018 through phylogenomic analysis of 351 genes across 61 taxa, uniting previously orphan lineages including collodictyonids, rigifilids, and mantamonads as a novel eukaryotic supergroup.[1] Within CRuMs, the primary constituent lineages are recognized at the order level, reflecting their morphological and molecular distinctiveness: Diphylleida (encompassing collodictyonids such as Collodictyon and Diphylleia), Rigifilida, Mantamonadida, and the newly erected Glissandrida.[1][2]- Diphylleida: Order authority attributed to Cavalier-Smith (1993) emend. Adl et al. (2012), comprising biflagellate predators with tubular mitochondrial cristae and a ventral feeding groove, represented by families like Collodictyonidae.[16]
- Rigifilida: Order established by Yabuki et al. (2012), featuring filose amoeboflagellates with a rigid pellicle, including genera Rigifila and Micronuclearia.[6]
- Mantamonadida: Order proposed by Glücksman et al. (2011), consisting of gliding biflagellates with a unique ventral pseudopodium, typified by the genus Mantamonas.
- Glissandrida: Order nov. defined by Yazaki et al. (2025), characterized by heterotrophic biflagellates with a sleeve-like flagellar transitional region and a single-layered pellicle, including the genus Glissandra.[2]