Carpediemonas

Last updated

Carpediemonas
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Phylum: Metamonada
Subphylum: Fornicata
Superclass: Carpediemonadia
Cavalier-Smith
Class: Carpediemonadea
Cavalier-Smith
Order: Carpediemonadida
Cavalier-Smith
Family: Carpediemonadidae
Genus: Carpediemonas
Ekebom, Patterson & Vørs, 1996 [1]
Type species
Carpediemonas membranifera
(Larsen & Patterson 1990) Ekebom, Patterson & Vørs 1996
Species
  • C. frisia
  • C. membranifera

Carpediemonas is genus of Metamonada, and belongs to the group Excavata. This organism is a unicellular flagellated eukaryote that was first discovered in substrate samples from the Great Barrier Reef. [2] Carpediemonas can be found in anaerobic intertidal sediment, where it feeds on bacteria. A feature of this species is the presence of a feeding groove, a characteristic of the excavates. Like most other metamonads, Carpediemonas does not rely on an aerobic mitochondrion to produce energy. Instead, it contains hydrogenosomes that are used to produce ATP. [3] This organism has two flagella: [3] a posterior one used for feeding on the substrate, and an anterior one that moves in a slower sweeping motion. [2] Carpediemonas is assigned to the fornicates, where similar Carpediemonas-like organisms are used in researching the evolution within excavates. [4] Although Carpediemonas is a member of the metamonads, it is unusual in the sense that it is free-living and has three basal bodies. [5]

Contents

Etymology

The name Carpediemonas originates from three Latin roots, with carpe meaning "seize", die meaning "the day", and the suffix of monas, indicating a unicellular organism. The organism was named after carpe diem , meaning "to seize the day", in honour of the wife of one of the authors, who had recently died. [6]

History of study

Carpediemonas was first discovered by Larsen and Patterson (1990) who identified it as a previously unidentified Percolomonas and provided the name Percolomonas membranifera. Larsen and Patterson treated this organism as a heterolobosean, because it would occasionally have four flagella and contain a longitudinal groove. However, they did not have any evidence that the non-dividing organisms had more than two flagella. The species also contained a pouch with threads that may be difficult to discern from flagella. Ekebom et al. (1996) then renamed the organism as Carpediemonas membranifera when it was found from substrate samples in the Great Barrier Reef and classified it as a metamonad. [2] Additionally, a metabolic relationship of Carpediemonas with prokaryotic communities was found in Carpediemonas frisia . C. frisia was found to release biomolecules that have been predigested. Prokaryotic communities would rely on C. frisia for incompletely digested organic material and the oxidation of various biomolecules. On the other hand, C. frisia relies on the prokaryotic organism, Deltaproteobacteria, for its hydrogen oxidizing activity. [7]

Habitat and ecology

Carpediemonas can be found in anaerobic intertidal sediments, where it feeds on bacteria. [3] It can be found co-existing with Cafeteria marsupialis in these anaerobic environments. [2]

Description

Ekebom et al. (1996) describes Carpediemonas as organisms with a size of approximately 5 μm long (with a range of 4–7.5 μm). Carpediemonas has a longitudinal depression that spans almost the entire ventral side of the cell. It often has two unequal flagella inserting to the anterior side of the ventral groove, but may sometimes have three or four flagella. The acronematic posterior flagellum is used in feeding and to attach to substrate, while the anterior flagellum beats less rapidly and in a slow sweeping motion. [2] Further studies by Simpson and Patterson (1999) go into greater detail about the flagella and describe the flagellar apparatus as having a third, barren basal body. Supporting the dorsal side of the cell is a microtubular fan with a microtubular root at the anterior end. On the ventral side, microtubules extending from different flagellar roots support the ventral groove. The anterior flagellum has a "9+2" axoneme. Simpson and Patterson described that in addition to the "9+2" axoneme, the posterior flagellum also has "three radiating lamellae of electron-dense material which form the central components of vanes". The first lamella arises from after the flagellar insertion and is directed ventrally. The second lamella originates opposite from the first lamella. The third lamella supports the third vane, which is located more distally and lies perpendicular to the other two vanes or lamellae. All three lamella have striations when viewed in a longitudinal section and these striations are perpendicular to the "9+2" axoneme. Carpediemonas contains a single ovate nucleus, located anteriorly in the cell. The nucleolus can also be found subcentrally within the nucleus. Carpediemonas also has no mitochondria, which is typical of metamonads. Instead, it has hydrogenosomes, likely derived from anaerobic mitochondria. It also contains a single Golgi dictyosome, located anteriorly, dorsally, and to the left of the flagellar apparatus. [3] The endoplasmic reticulum in this genus is mainly found near the periphery of the cell. Around the cytoplasm, food vacuoles containing bacterial contents can be found. [3] Also, three centrioles are present in Carpediemonas. [8]

Taxonomy

Carpediemonas is classified as an excavate because it has the characteristic feeding groove of the group. Within the excavates, Carpediemonas is assigned to the fornicates. In the fornicates, Carpediemonas-like organisms (CLOs) have allowed for the better understanding of the evolution of anaerobic excavates by studying their cytoskeletal traits and modified mitochondria. An example of a Carpediemonas-like organism that was used to study the evolutionary history within excavates is Kipferlia bialata. [4] According to recent research [9] this organism is able to replicate without some key proteins for replicating DNA.

DNA replication, chromosome segregation, and sex

A recent study using comparative genomics [10] has revealed extensive loss of the DNA replication and segregation protein complements within Metamonada and has highlighted that the genomes of C. membranifera and C. frisia are even further reduced. These genomes lack the DNA replication proteins of the origin recognition complex (ORC), Cdc6, some components of the GINS complex and some subunits of polymerases delta and epsilon, as well as most structural kinetochore subunits, a microtubule plus-end tracking complex and all subunits of the Ndc80 complex involved in chromosome segregation. ORC and Cdc6 are proteins in charge of replication initiation and licensing in eukaryotes, and their absence appears to indicate the existence of a non-standard and as-yet undescribed mechanism to start replication. The absence of Ndc80 complex proteins also suggest that a non-standard mechanism could be in place for chromosome attachment to microtubules for chromosome segregation. Carpediemonas is the first known eukaryote to possess such drastically altered DNA replication and segregation machineries. Since Carpediemonas reproduces, it is obvious that they do replicate their DNA and researchers have proposed a hypothesis on how replication starts. This hypothesis uses elements of processes observed in other species but takes into account the specific protein complements found in Carpediemonas. In short: replication is proposed to proceed by a Dmc1-dependent homologous recombination mechanism that does not require origins of replication and that is mediated by RNA:DNA hybrids. This hypothesis still needs to be experimentally proven. Sexual or parasexual reproduction have not been directly observed in Metamonada. However, the study confirms the conservation of key meiotic proteins in the group with the bonus finding that Carpediemonas species have homologs from the tmcB family and sperm-specific channel subunits, the latter only previously reported in Opisthokonta and three other protists. The presence of such proteins means that further investigations are required to understand if sex occurs, and if these proteins actually participate during sex and what their role could be.

Related Research Articles

<span class="mw-page-title-main">Flagellum</span> Cellular appendage functioning as locomotive or sensory organelle

A flagellum is a hair-like appendage that protrudes from certain plant and animal sperm cells, from fungal spores (zoospores), and from a wide range of microorganisms to provide motility. Many protists with flagella are known as flagellates.

The evolution of flagella is of great interest to biologists because the three known varieties of flagella – each represent a sophisticated cellular structure that requires the interaction of many different systems.

<span class="mw-page-title-main">Excavata</span> Supergroup of unicellular organisms belonging to the domain Eukaryota

Excavata is an extensive and diverse but paraphyletic group of unicellular Eukaryota. The group was first suggested by Simpson and Patterson in 1999 and the name latinized and assigned a rank by Thomas Cavalier-Smith in 2002. It contains a variety of free-living and symbiotic protists, and includes some important parasites of humans such as Giardia and Trichomonas. Excavates were formerly considered to be included in the now obsolete Protista kingdom. They were distinguished from other lineages based on electron-microscopic information about how the cells are arranged. They are considered to be a basal flagellate lineage.

<span class="mw-page-title-main">Parabasalid</span> Group of flagellated protists

The parabasalids are a group of flagellated protists within the supergroup Excavata. Most of these eukaryotic organisms form a symbiotic relationship in animals. These include a variety of forms found in the intestines of termites and cockroaches, many of which have symbiotic bacteria that help them digest cellulose in woody plants. Other species within this supergroup are known parasites, and include human pathogens.

<span class="mw-page-title-main">Metamonad</span> Phylum of excavate protists

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, 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.

<span class="mw-page-title-main">Retortamonad</span> Group of flagellates

The retortamonads are a small group of flagellates, most commonly found in the intestines of animals as commensals, although a free-living species called the Chilomastix cuspidata exists. They are grouped under the taxon Archezoa. They are usually around 5-20 μm in length, and all of their small subunit ribosomal RNA gene sequences are very similar to each other. There are two genera: Retortamonas with two flagella, and Chilomastix with four. In both cases there are four basal bodies anterior to a prominent feeding groove, and one flagellum is directed back through the cell, emerging from the groove.

The radial spoke is a multi-unit protein structure found in the axonemes of eukaryotic cilia and flagella. Although experiments have determined the importance of the radial spoke in the proper function of these organelles, its structure and mode of action remain poorly understood.

<i>Cafeteria roenbergensis</i> Species of single-celled organism

Cafeteria roenbergensis is a small bacterivorous marine flagellate. It was discovered by Danish marine ecologist Tom Fenchel and named by him and taxonomist David J. Patterson in 1988. It is in one of three genera of bicosoecids, and the first discovered of two known Cafeteria species. Bicosoecids belong to a broad group, the stramenopiles, also known as heterokonts (Heterokonta) that includes photosynthetic groups such as diatoms, brown, and golden algae, and non-photosynthetic groups such as opalinids, actinophryid "heliozoans", and oomycetes. The species is found primarily in coastal waters where there are high concentrations of bacteria on which it grazes. Its voracious appetite plays a significant role in regulating bacteria populations.

Trimastix is a genus of excavate protists, the sole occupant of the order Trimastigida. Trimastix are bacterivorous, free living and anaerobic. It was first observed in 1881 by William Kent. There are few known species, and the genus's role in the ecosystem is largely unknown. However, it is known that they generally live in marine environments within the tissues of decaying organisms to maintain an anoxic environment. Much interest in this group is related to its close association with other members of Preaxostyla. These organisms do not have classical mitochondria, and as such, much of the research involving these microbes is aimed at investigating the evolution of mitochondria.

<i>Malawimonas</i> Genus of micro-organisms

Malawimonas is genus of unicellular, heterotrophic flagellates with uncertain phylogenetic affinities. They have variably being assigned to Excavata and Loukozoa. Recent studies suggest they may be closely related to the Podiata.

<span class="mw-page-title-main">Jakobid</span> Clade of Eukaryotes

Jakobids are an order of free-living, heterotrophic, flagellar eukaryotes in the supergroup Excavata. They are small, and can be found in aerobic and anaerobic environments. The order Jakobida, believed to be monophyletic, consists of only twenty species at present, and was classified as a group in 1993. There is ongoing research into the mitochondrial genomes of Jakobids, which are unusually large and bacteria-like, evidence that Jakobids may be important to the evolutionary history of eukaryotes.

<i>Mastigamoeba</i> Genus of flagellar amoeboids

Mastigamoeba is a genus of pelobionts, and treated by some as members of the Archamoebae group of protists. Mastigamoeba are characterized as anaerobic, amitochondriate organisms that are polymorphic. Their dominant life cycle stage is as an amoeboid flagellate. Species are typically free living, though endobiotic species have been described.

<i>Jakoba</i> Genus of Eukaryotic Organisms

Jakoba is a genus in the taxon Excavata, and currently has a single described species, Jakoba libera described by Patterson in 1990, and named in honour of Dutch botanist Jakoba Ruinen.

Monocercomonoides is a genus of flagellate Excavata belonging to the order Oxymonadida. It was established by Bernard V. Travis and was first described as those with "polymastiginid flagellates having three anterior flagella and a trailing one originating at a single basal granule located in front of the anteriorly positioned nucleus, and a more or less well-defined axostyle". It is the first eukaryotic genus to be found to completely lack mitochondria, and all hallmark proteins responsible for mitochondrial function. The genus also lacks any other mitochondria related organelles (MROs) such as hydrogenosomes or mitosomes. Data suggests that the absence of mitochondria is not an ancestral feature, but rather due to secondary loss. Monocercomonoides sp. was found to obtain energy through an enzymatic action of nutrients absorbed from the environment. The genus has replaced the iron-sulfur cluster assembly pathway with a cytosolic sulfur mobilization system, likely acquired by horizontal gene transfer from a eubacterium of a common ancestor of oxymonads. These organisms are significant because they undermine assumptions that eukaryotes must have mitochondria to function properly. The genome of Monocercomonoides exilis has approximately 82 million base pairs, with 18 152 predicted protein-coding genes.

Stygiella /ˌstɪ.d͡ʒiˈɛ.lə/ is a genus of free-living marine flagellates belonging to the family Stygiellidae in the Jakobids (excavata).

<span class="mw-page-title-main">Ultrastructural identity</span>

Ultrastructural identity is a concept in biology. It asserts that evolutionary lineages of eukaryotes in general and protists in particular can be distinguished by complements and arrangements of cellular organelles. These ultrastructural components can be visualized by electron microscopy.

<i>Cafileria</i> Genus of marine protists

Cafileria is a genus of marine microscopic protists. It is monotypic, comprising the single species Cafileria marina, described in 2019 from Norway. It is part of a clade of heterotrophic flagellates that consume bacteria, known as Bicosoecida, a basal lineage of Stramenopiles. Due to its small size it is described as a nanoflagellate. It is the only organism where direct connections between mitochondria and the cell nucleus have been observed. Another peculiarity of C. marina is the change in shape of the Golgi apparatus during the cell cycle.

<span class="mw-page-title-main">Colponemid</span> Group of predatorial flagellates

Colponemids are free-living alveolates, unicellular flagellates related to dinoflagellates, apicomplexans and ciliates. They are predators of other small eukaryotes, found in freshwater, marine and soil environments. They do not form a solid clade, but a sparse group of deep-branching alveolate lineages.

Skoliomonas is a genus of anaerobic protists closely related to barthelonids, a small group of basal eukaryotes within the phylum Metamonada. It is a monotypic genus containing the sole species Skoliomonas litria. Members of this genus are informally named skoliomonads. They are found inhabiting hypersaline alkaline lakes in Tanzania and North America.

Barthelona is a genus of anaerobic protists. They are basal eukaryotes closely related to skoliomonads, within the phylum Metamonada. It is a monotypic genus containing the sole species Barthelona vulgaris. Members of this genus are informally known as barthelonids.

References

  1. J. Ekebom; D. J. Patterson; N. Vørs (1996). "Heterotrophic flagellates from coral reef sediments (Great Barrier Reef, Australia)". Archiv für Protistenkunde . 146 (3–4): 251–272. doi:10.1016/S0003-9365(96)80013-3.
  2. 1 2 3 4 5 Ekebom, J.; Patterson, D.J.; Vørs, N. (1996). "Heterotrophic Flagellates from Coral Reef Sediments (Great Barrier Reef, Australia)". Archiv für Protistenkunde. 146 (3–4): 251–272. doi:10.1016/s0003-9365(96)80013-3. ISSN   0003-9365.
  3. 1 2 3 4 5 Simpson, Alastair G.B.; Patterson, David J. (1999). "The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the "excavate hypothesis"". European Journal of Protistology. 35 (4): 353–370. doi:10.1016/s0932-4739(99)80044-3. ISSN   0932-4739.
  4. 1 2 Yubuki, Naoji; Simpson, Alastair G.B.; Leander, Brian S. (2013). "Comprehensive Ultrastructure of Kipferlia bialata Provides Evidence for Character Evolution within the Fornicata (Excavata)". Protist. 164 (3): 423–439. doi:10.1016/j.protis.2013.02.002. ISSN   1434-4610. PMID   23517666.
  5. "CARPEDIEMONADA". comenius.susqu.edu. Retrieved 2019-04-22.
  6. "Taxonomy – It Came from the Pond" . Retrieved 2019-04-22.
  7. Hamann, Emmo; Tegetmeyer, Halina E; Riedel, Dietmar; Littmann, Sten; Ahmerkamp, Soeren; Chen, Jianwei; Hach, Philipp F; Strous, Marc (2017-02-17). "Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations". The ISME Journal. 11 (5): 1205–1217. doi:10.1038/ismej.2016.197. ISSN   1751-7362. PMC   5437931 . PMID   28211847.
  8. Cavalier-Smith, T. (2003-11-01). "The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa". International Journal of Systematic and Evolutionary Microbiology. 53 (6): 1741–1758. doi: 10.1099/ijs.0.02548-0 . ISSN   1466-5026. PMID   14657102.
  9. "Microbe somehow survives without key proteins for replicating its DNA".
  10. Salas-Leiva, Dayana E.; Tromer, Eelco C.; Curtis, Bruce A.; Jerlström-Hultqvist, Jon; Kolisko, Martin; Yi, Zhenzhen; Salas-Leiva, Joan S.; Gallot-Lavallée, Lucie; Williams S., Williams S.; Kops, Geert J. P. L.; Archibald, John M.; Simpson, Alastair G. B.; Roger, Andrew J. (2021). "Genomic analysis finds no evidence of canonical eukaryotic DNA processing complexes in a free-living protist". Nature Communications. 12 (1): 6003. Bibcode:2021NatCo..12.6003S. doi:10.1038/s41467-021-26077-2. PMC   8516963 . PMID   34650064.