Nemertean taxonomy—Implementing changes in the higher ranks, dismissing Anopla and Enopla

Strand, Malin; Norenburg, Jon L.; Alfaya, José E. F.; Fernández-Álvarez, Fernando Ángel; Andersson, Håkan S.; Andrade, Sónia C. S.; Bartolomaeus, Thomas; Beckers, Patrick; Bigatti, Gregório; Cherneva, Irina A.; Chernyshev, A. V.; Chung, Bonghoon; Döhren, Jörn von; Giribet, Gonzalo; Gonzalez-Cueto, Jaime; Herrera-Bachiller, Alfonso; Hiebert, Terra C.; Hookabe, Natsumi; Junoy, Juan; Kajihara, Hiroshi; Krämer, Daria; Kvist, Sebastian; Magarlamov, Timur Yu.; Maslakova, Svetlana A.; Mendes, Cecili B.; Okazaki, Robert K.; Sagorny, Christina; Schwartz, Megan L.; Sun, Shichun; Sundberg, Per; Turbeville, James M.; Xu, Cong-Mei

doi:10.1111/zsc.12317

Cited by 27 publications

(12 citation statements)

References 4 publications

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“…It belongs to the disputed superphylum Lophotrochozoa, which contains one third of all marine animals, including sensu stricto polychaetes, mollusks, brachiopods and phoronids [ 1 , 2 , 3 ]. A recently-proposed system has established three nemertean classes: Paleonemertea, Pilidiophora and Hoplonemertea [ 4 ]. All three feature an eversible proboscis, but hoplonemerteans uniquely possess a hardened needle-like proboscis tip that can pierce the prey cuticle, as shown for the topic of this study: Amphiporus lactifloreus ( Figure 1 ).…”

Section: Introductionmentioning

confidence: 99%

Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus

et al. 2020

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Nemerteans (ribbon worms) employ toxins to subdue their prey, but research thus far has focused on the small-molecule components of mucus secretions and few protein toxins have been characterized. We carried out a preliminary proteotranscriptomic analysis of putative toxins produced by the hoplonemertean Amphiporus lactifloreus (Hoplonemertea, Amphiporidae). No variants were found of known nemertean-specific toxin proteins (neurotoxins, cytotoxins, parbolysins or nemertides) but several toxin-like transcripts were discovered, expressed strongly in the proboscis, including putative metalloproteinases and sequences resembling sea anemone actitoxins, crown-of-thorn sea star plancitoxins, and multiple classes of inhibitor cystine knot/knottin family proteins. Some of these products were also directly identified in the mucus proteome, supporting their preliminary identification as secreted toxin components. Two new nemertean-typical toxin candidates could be described and were named U-nemertotoxin-1 and U-nemertotoxin-2. Our findings provide insight into the largely overlooked venom system of nemerteans and support a hypothesis in which the nemertean proboscis evolved in several steps from a flesh-melting organ in scavenging nemerteans to a flesh-melting and toxin-secreting venom apparatus in hunting hoplonemerteans.

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Section: Introductionmentioning

confidence: 99%

Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus

et al. 2020

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“…According to recent phylogenetic analyses [51,52], Palaeonemertea is a sister group (classsee [53]) to other nemerteans (or Neonemertea [54]). The planuliform larva of palaeonemerteans resembles a decidula in appearance [38,40,55] despite the lack of a transitory epidermis composed of large multiciliated cells [35].…”

Section: Apical Organs Of the Palaeo-and Hoplonemertean Larvaementioning

confidence: 99%

Does the frontal sensory organ in adults of the hoplonemertean Quasitetrastemma stimpsoni originate from the larval apical organ?

2020

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Background: The apical organ is the most prominent neural structure in spiralian larvae. Although it has been thoroughly investigated in larvae of the class Pilidiophora in phylum Nemertea, studies on its structure in other nemertean larvae are limited. Most adult hoplonemertean worms have a frontal organ located in a position corresponding to that of the larval apical organ. The development and sensory function of the frontal organ has not been thoroughly characterized to date. Results: The apical organ in the early rudiment stage of Quasitetrastemma stimpsoni larvae consists of an apical plate enclosed by ducts of frontal gland cells and eight apical neurons. The apical plate is abundantly innervated by neurites of apical neurons. During the late rudiment stage, the larval apical organ has external innervation from below by two subapical-plate neurons, along with 11 apical neurons, and its plate contains serotonin-like immunoreactive (5-HT-lir) cells. In the vermicular stage (free-swimming juvenile), the number of apical neurons is reduced, and their processes are resorbed. Serotonin is detected in the apical plate with no visible connection to apical neurons. In adult worms, the frontal organ has a small apical pit with openings for the frontal gland ducts. The organ consists of 8 to 10 densely packed 5-HT-lir cells that form the roundish pit. Conclusions: Although the ultrastructure of the Q. stimpsoni larval apical organ closely resembles that of the apical organ of Polycladida larvae, the former differs in the presence of flask-shaped neurons typical of Spiralia. Significant differences in the structure of the apical organs of hoplonemertean and pilidia larvae point to two different paths in the evolutionary transformation of the ancestral apical organ. Ultrastructural and immunoreactive analyses of the apical organ of a hoplonemertean larva in the late rudiment and vermicular stages and the frontal organ of the adult worms identified common morphological and functional features. Thus, we hypothesize that the larval apical organ is modified during morphogenesis to form the adult frontal organ, which fulfills a sensory function in the hoplonemertean worm. This unique developmental trait distinguishes the Hoplonemertea from other nemertean groups.

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“…Traditionally, the two suborders, Anopla and Enopla, have been used following Johnston’s (1837) [ 12 ] grouping that is based primarily on the absence or presence of the stylet apparatus in the proboscis. Recently, these suborders were dismissed [ 13 ] and instead three classes (natural groups) are maintained from the compiled evidence of the last 15 years: Palaeonemertea, Pilidiophora, and Hoplonemertea. The main morphological features that are used for further classification are muscle layers in the body wall, armament of proboscis (Hoplonemertea), and placement of mouth opening.…”

Section: Taxonomy and Phylogenymentioning

confidence: 99%

“… Schematic phylogenetic tree over the Nemertea phylum with names as proposed by Strand et al [ 13 ]. Current intraphylum theories suggest relatively closer relationship between Pilidiophora and Hoplonemertea with Palaeonemertea outside this branch.…”

Section: Figurementioning

confidence: 99%

The Toxins of Nemertean Worms

Göransson

Jacobsson

Strand

et al. 2019

Toxins

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Most ribbon worms (phylum: Nemertea) are found in marine environments, where they act as predators and scavengers. They are characterized by an eversible proboscis that isused to hunt for prey and thick mucus covering their skin. Both proboscis and epidermal mucus mediate toxicity to predators and preys. Research into the chemical nature of the substances that render toxicity has not been extensive, but it has nevertheless led to the identification of several compounds of potential medicinal use or for application in biotechnology. This review provides a complete account of the current status of research into nemertean toxins.

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Nemertean taxonomy—Implementing changes in the higher ranks, dismissing Anopla and Enopla

Cited by 27 publications

References 4 publications

Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus

Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus

Does the frontal sensory organ in adults of the hoplonemertean Quasitetrastemma stimpsoni originate from the larval apical organ?

The Toxins of Nemertean Worms

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