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Metamonad

Clade of excavate protists

Parabasalia
Preaxostyla
Anaeramoebae
BaSk
Centrosomea Chatton Villeneuve 1937
Metamonadina Grassé 1952
Polymastigota Butschli 1884
Tetramastigota Hulsmann & Hausmann 1994

The metamonads are a large group of flagellate amitochondriate microscopic eukaryotes. They include the retortamonads, diplomonads, parabasalids, oxymonads, and a range of more poorly studied taxa, most of which are free-living flagellates. All metamonads are anaerobic (many being aerotolerant anaerobes), and most members of the four groups listed above are symbiotes or parasites of animals, as is the case with Giardia lamblia which causes diarrhea in mammals.

Characteristics

A number of parabasalids and oxymonads are found in termite guts, and play an important role in breaking down the cellulose found in wood. Some other metamonads are parasites.

These flagellates are unusual in lacking aerobic mitochondria. Originally they were considered among the most primitive eukaryotes, diverging from the others before mitochondria appeared. However, they are now known to have lost aerobic mitochondria secondarily, and retain both organelles and nuclear genes derived ultimately from the mitochondrial endosymbiont genome. Mitochondrial relics include hydrogenosomes, which produce hydrogen (and make ATP), and small structures called mitosomes.

It now appears the Metamonada are, together with Malawimonas, sister clades of the Podiata.

All of these groups have flagella or basal bodies in characteristic groups of four (or more, in parabasalids), which are often associated with the nucleus, forming a structure called a karyomastigont. In addition, genera such as Carpediemonas and Trimastix are now known to be close relatives of the retortamonad-diplomonad lineage and the oxymonads, respectively. Most of the closer relatives of the retortamonad-diplomonad lineage actually have two flagella and basal bodies.

Classification

The metamonads were thought to make up part of the Excavata, a proposed eukaryotic supergroup including flagellates with feeding grooves and their close relatives. Their relationships are uncertain, and they do not always appear together on molecular trees. Current opinion is that Excavata is not a monophyletic group, but it might be paraphyletic.

Metamonada were once again proposed to be basal eukaryotes in 2018.

A view of the metamonad taxonomy is:

Clade Metamonada
- Phylum Fornicata
  - Order Diplomonadida
    - Family Hexamitidae
      - Subfamily Hexamitinae
      - Subfamily Giardiinae
  - Order Retortamonadida (paraphyletic)
    - Family Retortamonadidae (paraphyletic)
  - Order Dysnectida
    - Family Dysnectidae
  - Family Caviomonadidae
  - Family Kipferliidae
  - Genus Aduncisulcus
  - Genus Carpediemonas
  - Genus Ergobibamus
  - Genus Hicanonectes
- Phylum Parabasalia
  - Class Hypotrichomonadea
    - Order Hypotrichomonadida
      - Family Hypotrichomonadidae
  - Class Pimpavickea
    - Order Pimpavickida
      - Family Pimpavickidae
  - Class Trichomonadea
    - Order Honigbergiellida
      - Family Hexamastigidae
      - Family Honigbergiellidae
      - Family Cthulhuidae
      - Family Tetratrichomastigidae
    - Order Trichomonadida
      - Family Lacusteriidae
      - Family Trichomonadidae
      - Family Incertae sedis
        
        Genus Pseudotrichomonas
        
        Genus †Paleotrichomones
  - Clade "Tla"
    - Class Lophomonadea
      - Order Lophomonadida
        
        Family Lophomonadidae
    - Class Trichonymphea
      - Order Trichonymphida
        
        Family Barbulanymphidae
        
        Family Hoplonymphidae
        
        Family Retractinymphidae
        
        Family Spirotrichosomidae
        
        Family Staurojoeninidae
        
        Family Teranymphidae
        
        Family Trichonymphidae
        
        Family †Burmanymphidae
  - Clade "Cadamassta"
    - Class Cristamonadea
      - Order Calonymphida
        
        Family Calonymphidae
        
        Family Deltotrichonymphidae
        
        Family Mixotrichidae
      - Order Devescovinida
        
        Family Devescovinidae
      - Order Gigantomonadida
        
        Family Gigantomonadidae
      - Order Incertae sedis
        
        Genus Cyclojoenia
        
        Genus Joenia
        
        Genus Joenina
        
        Genus Joenoides
        
        Genus Joenopsis
        
        Genus Pachyjoenia
        
        Genus Parajoenopsis
        
        Genus Placojoenia
        
        Genus Projoenia
    - Class Dientamoebea
      - Order Dientamoebida
        
        Family Dientamoebidae
    - Class Monocercomonadea
      - Order Monocercomonadida
        
        Family Monocercomonadidae
    - Class Simplicimonadea
      - Order Simplicimonadida
        
        Family Simplicimonadidae
    - Class Tritrichomonadea
      - Order Tritrichomonadida
        
        Family Tritrichomonadidae
    - Class Spirotrichonymphea
      - Order Cononymphida
        
        Family Cononymphidae
      - Order Holomastigotoidida
        
        Family Holomastigotoididae
      - Order Spirotrichonymphida
        
        Family Brugerollinidae
        
        Family Fraterculidae
        
        Family Holomastigotidae
        
        Family Spirotrichonymphidae
  - Class Incertae sedis
    - Genus Chilomitus
    - Genus Rhizonympha
    - Genus Tricercomitus
    - Genus Trichocovina
- Phylum Preaxostyla
  - Order Oxymonadida
    - Family Oxymonadidae
    - Family Pyrsonymphidae
    - Family Streblomastigidae
    - Family Saccinobaculidae
    - Family Polymastigidae
  - Order Trimastigida
    - Family Trimastigidae
  - Order Paratrimastigida
    - Family Paratrimastigidae
- Phylum Anaeramoebae
  - Family Anaeramoebidae
- Clade BaSk
  - Genus Barthelona
  - Genus Skoliomonas

Evolution

Within Metamonada, two main branches are recovered in recent phylogenetic analyses. One branch contains the Parabasalia and the closely related anaeramoebae. The other branch contains two large groups: the Fornicata, which is closely related to barthelonids and the recently isolated Skoliomonas; and the Preaxostyla.

A 2023 study found it likely that Metamonada is a paraphyletic group at the base of Eukaryota, meaning their anaerobic metabolism possibly represents the ancestral condition in eukaryotes (similar to what the Archezoa-Metakaryota hypothesis proposed) and that aerobic mitochondria might not have the same origin as hydrogenosomes.

References

(2023-04-28). "An excavate root for the eukaryote tree of life". Science Advances.
(2016-06-01). "187-gene phylogeny of protozoan phylum Amoebozoa reveals a new class (Cutosea) of deep-branching, ultrastructurally unique, enveloped marine Lobosa and clarifies amoeba evolution". Molecular Phylogenetics and Evolution.
Cavalier-Smith T. (November 2003). "The excavate protozoan phyla Metamonada Grassé emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa". Int. J. Syst. Evol. Microbiol..
(2018). "Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements". iScience.
Adl, Sina M.. (2019). "Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes". Journal of Eukaryotic Microbiology.
Boscaro, Vittorio. (2024). "Updated classification of the phylum Parabasalia". Journal of Eukaryotic Microbiology.
Cavalier-Smith, Thomas. (2013-05-01). "Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa". European Journal of Protistology.
Vargová, Romana. (2022-05-19). "Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates". Frontiers in Microbiology.
Jørgensen, Anders. (2007-04-18). "Phylogeny of Spironucleus (Eopharyngia: Diplomonadida: Hexamitinae)". Protist.
Kolisko, Martin. (2008-07-15). "Molecular phylogeny of diplomonads and enteromonads based on SSU rRNA, alpha-tubulin and HSP90 genes: Implications for the evolutionary history of the double karyomastigont of diplomonads". BMC Evolutionary Biology.
Martínez-Díaz, Rafael A.. (2001). "First report of the genus Retortamonas (Sarcomastigophora: Retortamonadidae) in birds". Memórias do Instituto Oswaldo Cruz.
Stairs, Courtney W.. (2021-12-20). "Anaeramoebae are a divergent lineage of eukaryotes that shed light on the transition from anaerobic mitochondria to hydrogenosomes". Current Biology.
Yazaki, Euki. (2020-09-09). "Barthelonids represent a deep-branching metamonad clade with mitochondrion-related organelles predicted to generate no ATP". Proceedings of the Royal Society B: Biological Sciences.
Eglit, Yana. (2024). "Characterization of Skoliomonas gen. nov., a haloalkaliphilic anaerobe related to barthelonids (Metamonada)". Journal of Eukaryotic Microbiology.
Zhang, Qianqian. (2015-09-01). "Marine Isolates of Trimastix marina Form a Plesiomorphic Deep-branching Lineage within Preaxostyla, Separate from Other Known Trimastigids (Paratrimastix n. gen.)". Protist.
Cavalier-Smith, Thomas. (2022-05-01). "Ciliary transition zone evolution and the root of the eukaryote tree: implications for opisthokont origin and classification of kingdoms Protozoa, Plantae, and Fungi". Protoplasma.
Poinar, George. (2009-10-01). "Early Cretaceous protist flagellates (Parabasalia: Hypermastigia: Oxymonada) of cockroaches (Insecta: Blattaria) in Burmese amber". Cretaceous Research.
(9 August 2024). "Extreme mitochondrial reduction in a novel group of free-living metamonads". Nature Communications.

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