The Toxins of Nemertean Worms
Abstract
:1. Introduction
2. Taxonomy and Phylogeny
3. Anatomy
4. Early Descriptions of Ribbon Worms and Their Toxins
5. Ribbon Worm Toxins
5.1. Pyridine Alkaloids
5.2. Tetrodotoxin (TTX)
5.3. Peptide Toxins
5.3.1. Cerebratulus Toxins
B-neurotoxins
Cerebratulus A-Toxins
5.3.2. Parborlasia Toxins
5.3.3. Lineus Toxins
5.3.4. Other Peptide and Protein Toxins
6. The Ecological Roles of Nemertean Toxins
6.1. Nemerteans as Preys
6.2. Nemerteans as Predators and Scavengers
6.3. Commensal Nemerteans
7. Conclusions and Future Outlook
Funding
Acknowledgments
Conflicts of Interest
References
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Compound | Barnacle Larvae Settlement Inhibition IC50 (μM) | Barnacle Larvae Median Lethal Concentration IL50 (μM) | Crayfish Acute Paralytic Dose PD50 (μg) |
---|---|---|---|
2,3′-bipyridyl | 4.1 (3.2–5.3) a | 1.9 (1.0–4.3) | 0.88 (0.71–1.1) |
Anabaseine | 1.2 (0.91–1.7) | 2 | 3.6 (3.1–4.1) |
Nemertelline | 3.2 (1.8–6.0) | - | >120 |
Anabasine | 3.0 (1.5–4.9) | - | 3.9 (3.4–4.5) |
Species | Origin | Toxin | Sample | Extraction and Analysis | Source |
---|---|---|---|---|---|
Class Hoplonemertea | Order Monostilifera | ||||
Amphiporus angulatus | NH + ME shores, USA | Anabaseine | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5,17] |
Amphiporus angulatus | NH + ME shores, USA | Anabaseine | Whole body | Chromatogr - alkal CHCl3 extr | [36] |
Amphiporus angulatus | NH + ME shores, USA | Nemertelline | Whole body | Chromatogr - alkal CHCl3 extr | [36] |
Amphiporus angulatus | NH + ME shores, USA | 2,3′-bipyridyl | Whole body | Chromatogr - alkal CHCl3 extr | [36] |
Amphiporus angulatus | NH + ME shores, USA | 3-methyl-2,3′-bipyridyl | Whole body | Chromatogr - alkal CHCl3 extr | [36,40] |
Amphiporus angulatus | Not stated | Bipyridyl toxins | Live animal | Not stated | [53] |
Amphiporus angulatus | Eastport, MA, USA. | 2,3′-bipyridyl, nemertelline + 4 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Amphiporus bimaculatus | San Juan Island, Washington, USA. | Unidentified pyridyl | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Amphiporus cruentatus | Woods hole, MA, USA. | 5 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Amphiporus formidabilis | San Juan Island, Washington, USA. | 3 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Amphiporus lactifloreus | Not stated | Low anabaseine activity | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [17] |
Amphiporus lactifloreus | Not stated | Low anabaseine activity | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5] |
Amphiporus lactifloreus | Bangor, Wales, UK | Anabasine | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Amphiporus ochraceus | Not stated | None found | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5,17] |
Amphiporus ochraceus | Woods hole, MA, USA | 5 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Argonemertes dendyi | Tomales bay, CA, USA | 1 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Carcinonemertes errans | Bodega bay, CA, USA | None found | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Emplectonema gracile | San Juan Island, WA, USA | Possibly 1 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Emplectonema gracile | San Juan Island, WA, USA | 1 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Emplectonema neesi | Bangor, Wales, UK | None found | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Fasciculonemertes arenicola | Los Molles, Chile | 5 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Geonemertes pelaensis | Miami, FL, USA | 1 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Malacobdella grossa | Not stated | None found | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5,17] |
Nipponnemertes pulchra a | Helsingør, Dk | 1 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Whole body | Al2O3 chrom-alkal CHCl3 extr. | [35] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Body w.o. proboscis | MS + UV - DMAB deriv | [5,17] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Anterior proboscis | MS + UV - DMAB deriv | [5,17] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Median proboscis | MS + UV - DMAB deriv | [5,17] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Posterior proboscis | MS + UV - DMAB deriv | [5,17] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Periph part body wall | MS + UV - DMAB deriv | [17] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Periph part body wall | MS + UV - DMAB deriv | [5] |
Paranemertes peregrina | San Juan Island, WA, USA | Low anabaseine | Body core tissues | MS + UV - DMAB deriv | [17] |
Paranemertes peregrina | San Juan Island, WA, USA | Low anabaseine | Body core tissues | MS + UV - DMAB deriv | [5] |
Paranemertes peregrina | San Juan Island, WA, USA | Anabaseine | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5,17] |
Paranemertes peregrina | Bodega Bay, CA, USA | 2 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Prosadenoporus californiensis b | Tomales Bay, CA, USA | 2 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Prostoma graecense c | Not stated | Possibly anabaseine | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5,17] |
Tetrastemma candidum | Woods hole, CA, USA | 1 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Tetrastemma reticulatum | San Juan Island, WA, USA | 1 unidentified | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Tetrastemma worki | Not stated | Anabaseine | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5,17] |
Zygonemertes virescens | Not stated | None found | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5] |
Zygonemertes virescens | Woods hole, MA, USA | Anabasine | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Class Palaeonemertea | |||||
Carinoma sp. | Not stated | None found | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5] |
Carinoma tremaphoros d | Woods hole, MA, USA. | Not reported | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Cephalothrix spiralis d,e | Not stated | None found | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5,17] |
Class Pilidiophora | Order Heteronemertea | ||||
Cerebratulus lacteus | Woods hole, MA, USA. | None found | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5,17] |
Cerebratulus lacteus | Boston, MA, USA | None found | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Lineus ruber | Not stated | Anabaseine/Nemertine Below detection level | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [17] |
Lineus ruber | NH + ME shores, USA | Anabaseine/Nemertine Below detection level | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5] |
Lineus sanguineus f | Not stated | Anabaseine/Nemertine Below detection level | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5,17] |
Lineus viridis | Not stated | Anabaseine/Nemertine | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [17] |
Lineus viridis | NH + ME shores, USA | Anabaseine/Nemertine | Whole body | TLC - alkal CHCl3 extr., DMAB deriv. | [5] |
Lineus viridis | Woods hole, MA, USA | None found | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Micrura leidyi | Not stated | Anabaseine/Nemertine | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [17] |
Micrura leidyi | Woods hole, MA, USA | None found | Whole body Frozen | TLC - alkal CHCl3 extr | [38] |
Micrura leidyi | Not stated | Anabaseine/Nemertine Below detection level | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5] |
Parvicirrus dubius g | Not stated | Anabaseine/Nemertine Below detection level | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5] |
Siphonenteron bicolour h | Not stated | Anabaseine/Nemertine Below detection level | Whole body | TLC - alkal CHCl3 extr - DMAB deriv | [5] |
Siphonenteron bicolour h | Woods hole, MA, USA | None found | Whole body Frozen | TLC - alkal/acid CHCl3 extr | [38] |
Species | Origin | Toxin/-s | Sample | Extraction and Analysis | Ref |
---|---|---|---|---|---|
Class Hoplonemertea | Order Monostilifera | ||||
Amphiporus lactifloreus | Llandudno, Wales, UK, or Rhosneigr, Wales, UK | TTX-like cpds | Acidic whole body extract | UV spectroscopy and HPLC | [72] |
Amphiporus sp. | Akkeshi Bay, Hokkaido, Jpn | TTX + analogs | Acidic whole body extract | Defatted, charcoal purif, HPLC and GC-MS-C9 base | [69] |
Nipponnemertes bimaculata a | Peter the Great Bay, Rus/Jpn | Very low TTX | Acidic MeOH extract | HPLC-MS/MS | [83] |
Malacobdella japonica | Akkeshi Bay, Hokkaido, Jpn | TTX + analogs Anhydro-TTX | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Malacobdella grossa | Peter the Great Bay, Rus/Jpn | Antimicrobial activity. No TTX. | Bacteria - whole body homogenate | Confocal laser microscopy after TTX antibody labeling | [80] |
Nemertellina yamaokai | Akkeshi Bay, Hokkaido, Jpn | None found | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Nipponnemertes punctatula | Otsuchi Bay, Iwate, Jpn | TTX, epi-, anhydro-TTX | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Paranemertes sp. | Peter the Great Bay, Rus/Jpn | None found | Acidic methanol extract | HPLC-MS/MS | [83] |
Quasitetrastemma nigrifrons b | Akkeshi Bay, Hokkaido, Jpn | None found | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Quasitetrastemma stimpsoni c | Akkeshi Bay, Hokkaido, Jpn | (TTX and analogues) Not analyzed | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Quasitetrastemma stimpsoni c | Peter the Great Bay, Rus/Jpn | Bact. cultures Antimicrob activity. TTX. | Bacteria from whole body homogenate | Confocal laser microscopy after TTX antibody labeling | [80] |
Quasitetrastemma stimpsoni | Peter the Great Bay, Rus/Jpn | Very low TTX | Acidic methanol extract | HPLC-MS/MS | [83] |
Class Palaeonemertea | |||||
Cephalothrix linearis | Shimoda, Shizuoka, Jpn | TDA-like, TTX, anhydro-, epi-TTX | Proboscis, body | SEC, TLC, el.phoresis, HPLC, GC-C9 base | [65] |
Cephalothrix linearis | Shimoda, Shizuoka, Jpn | TDA-like | Handling stimulus secretion | SEC, TLC, el.phoresis, HPLC, GC-C9 base | [65,66] |
Cephalothrix rufifrons | Llandudno, Wales, UK, or Rhosneigr, Wales, UK | TTX-like cpds | Acidic whole body extract | UV spectroscopy and HPLC | [72] |
Cephalotrix rufifrons d | Cornwall, UK | None in extract, but TTX in bacteria isolate | Acidic whole body extract and bacteria isolates | HPLC-MS/MS of extract and isolates | [85] |
Cephalothrix simula | Hiroshima Bay, Jpn | TTX, epi-, anhydro-TTX | Acidic whole body extract | Defatted, charcoal purif, HPLC and GC-MS-C9 base | [69] |
Cephalothrix simula | Akkeshi Bay, Hokkaido, Jpn | TTX, epi-, anhydro-TTX | Acidic whole body extract | Defatted, charcoal purif, HPLC and GC-MS-C9 base | [69] |
Cephalothrix simula | Otsuchi Bay, Iwate, Jpn | TTX, epi-, anhydro-TTX | Acidic whole body extract | Defatted, charcoal purif, HPLC and GC-MS- C9 base | [69] |
Cephalothrix simula e | Peter the Great Bay, Rus/Jpn | TTX-Bacillus sp. | Bacteria isolates | Immunovisualization | [78,79] |
Cephalothrix simula | Peter the Great Bay, Rus/Jpn | 7 TTX derivatives | Acidic MeOH extract | HPLC-MS/MS | [83] |
Cephalotrix simula | Cornwall, UK | TTX and derivatives | Acidic whole body extract and bacteria isolates | HPLC-MS/MS of extract and isolates | [85] |
Cephalothrix sp. | Hiroshima Bay, Jpn | TTX, epi-, anhydro-TTX | Acidic whole body extract | Defatted, SEC, IEC. TLC, HPLC, GCMS-C9 base | [67] |
Cephalothrix sp. | Hiroshima Bay, Jpn | TTX, epi-, anhydro-TTX | Whole body, frozen | Activated charcoal, SEC, IEC, cryst from acidic CH3OH soln, GCMS-C9 base, NMR + MS | [68] |
Cephalothrix sp. | Hiroshima Bay, Jpn | TTX | Whole body, cross-section | Anti-TTX antibodies | [81] |
Tubulanus annulatus | Cornwall, UK | None found | Acidic whole body extract and bacteria isolates | HPLC-MS/MS of extract and isolates | [85] |
Tubulanus polymorphus f | Not stated | TTX | Not stated | Immunostaining | [87] |
Tubulanus punctatus | Seto Inland sea Hiroshima, Jpn | Anhydro-TTX | Whole body | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [64] |
Tubulanus punctatus | Peter the Great Bay, Rus/Jpn | Very low TTX | Acidic MeOH extract | HPLC-MS/MS | [83] |
Class Pilidiophora | Order Heteronemertea | ||||
Cerebratulus marginatus | Peter the Great Bay, Rus/Jpn | None found | Acidic MeOH extract | HPLC-MS/MS | [83] |
Dushia atra f | Not stated | TTX | Not stated | Immunostaining | [87,88] |
Kulikovia alborostrata | Peter the Great Bay, Rus/Jpn | Very low TTX | Acidic MeOH extract | HPLC-MS/MS | [83] |
Kulikovia manchenkoi | Peter the Great Bay, Rus/Jpn | TTX + 3 deriv | Acidic MeOH extract | HPLC-MS/MS | [83] |
Lineus alborostratus | Akkeshi Bay, Hokkaido, Jpn | TTX, anhydro-, epi-TTX | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Lineus alborostratus | Peter the Great Bay, Rus/Jpn | TTX | Whole body | Immunostaining | [82] |
Lineus alborostratus | Peter the Great Bay, Rus/Jpn | Bact cultured for TTX. Antimicrob activity. | Bacteria from whole body homogenate | Confocal laser microscopy after TTX antibody labeling | [80] |
Lineus bilineatus | Akkeshi Bay, Hokkaido, Jpn | None found | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Lineus fuscoviridis | Seto Inland sea, Hiroshima, Jpn | TTX, anhydro-TTX | Whole body | Defatted, SEC, IEC. TLC, HPLC., GC-MS-C9 base | [64] |
Lineus longissimus | Llandudno, Wales, UK, or Rhosneigr, Wales, UK | TTX-like cpds | Acidic whole body extract and mucus | UV spectroscopy and HPLC | [72] |
Lineus longissimus | Koster Fiord, Swe, and Millport, Scot, UK | <5 kDa cpd | Mucus + Vibrio cultures | Various purification methods | [25] |
Lineus ruber | Llandudno, Wales, UK, or Rhosneigr, Wales, UK | TTX-like cpds | Acidic whole body extract | UV spectroscopy and HPLC | [72] |
Lineus sanguineus g | Llandudno, Wales, UK, or Rhosneigr, Wales, UK | TTX-like cpds | Acidic whole body extract | UV spectroscopy and HPLC | [72] |
Lineus torquatus | Akkeshi Bay, Hokkaido, Jpn | TTX, anhydro-, epi-TTX | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Lineus viridis | Llandudno, Wales, UK, or Rhosneigr, Wales, UK | TTX-like cpds | Acidic whole body extract | UV spectroscopy and HPLC | [72] |
Micrura akkeshiensis | Akkeshi Bay, Hokkaido, Jpn | None found | Acidic whole body extract | Defatted, charcoal purif, HPLC, GC-MS-C9 base | [69] |
Micrura bella | Peter the Great Bay, Rus/Jpn | None found | Acidic MeOH extract | HPLC-MS/MS | [83] |
Micrura verrilli f | Not stated | TTX | Not stated | Immunostaining | [87,88] |
Nipponomicrura uchidai | Peter the Great Bay, Rus/Jpn | None found | Acidic methanol extract | HPLC-MS/MS | [83] |
Riseriellus occultus | Llandudno, Wales, UK, or Rhosneigr, Wales, UK | TTX-like cpds | Acidic whole body extract | UV spectroscopy and HPLC | [72] |
Yininemertes pratensis | Haengjunaru, Han river Estuary, South Korea | TTX + analogs, derivatives. Tox cpd mass 291.1 | EtOH extract | Dry homogenate lysis in pure EtOH, hydrophobic HPLC, MALDI-TOF | [84] |
Class Pilidiophora | Genus Hubrechtella | ||||
Hubrechtella juliae | Peter the Great Bay, Rus/Jpn | Bact cultured for TTX. Antimicrob activity. | Bacteria from whole body homogenate | Confocal laser microscopy after TTX antibody labeling | [80] |
Residue | AA | Modification | Effect | Source |
---|---|---|---|---|
1 | Ala | Extra Met-1 | 35-40% of native | [100] |
3 | Ala | Ser (+8 Ser) | x2 activity | [101] |
Gly (+8 Gly) | Slightly less active | [101] | ||
5 | Trp | HNB a w Trp 30, 1 eq. | Slightly less active | [92] |
HNB w Trp 30, 2 eq. | Inactive | [93] | ||
8 | Ala | Ser (+8 Ser) | x2 activity | [101] |
Gly (+8 Gly) | Slightly less active | [101] | ||
9 | Tyr | Nitration | Inactive | [92] |
10 | Hyp | Pro | Active | [101] |
12 | Cys | Reduction (all Cys) | Inactive | [94] |
13 | Glu | Gly | Active | [102] |
Ala | Active | [102] | ||
Gln | Active | [102] | ||
16 | Cys | Reduction (all Cys) | Inactive | [94] |
17 | Arg | Gln | Inactive | [102] |
Ala | Inactive | [102] | ||
Lys | Inactive | [102] | ||
18 | Lys | Gln | Active | [103] |
Gln + Gln 19 | Slightly less active | [103] | ||
19 | Lys | Gln + Gln 18 | Slightly less active | [103] |
21 | Asp | Ala | Active | [102] |
Asn | Active | [102] | ||
Pro | 75% helix reduction. 10-fold reduction in activity | [102] | ||
22 | Leu | Asp | Active | [103] |
23 | Cys | Reduction (all Cys) | Inactive | [94] |
25 | Arg | Gln | 400-fold reduction | [102] |
Lys | Slightly less active | [102] | ||
26 | Cys | Reduction (all Cys) | Inactive | [94] |
29 | Lys | Asn | Active | [103] |
30 | Trp | HNB | Inactive | [93] |
Ser | 40-fold reduction | [103] | ||
Tyr | Active | [103] | ||
Phe | Active | [103] | ||
HNB with Trp 5, 1 eq. | Slightly less active | [93] | ||
HNB with Trp 5, 2 eq. | Inactive | [93] | ||
33 | Lys | Asn | Active | [103] |
34 | Arg | Gln | 20-fold reduction. Structure destabilized. | [102] |
Ala | 80-fold reduction | [102] | ||
37 | Cys | Reduction (all Cys) | Inactive | [94] |
41 | Cys | Reduction (all Cys) | Inactive | [94] |
48 | Cys | Reduction (all Cys) | Inactive | [94] |
52 | Cys | Reduction (all Cys) | Inactive | [94] |
53 | Lys | Truncation | Active | [102] |
54 | Lys | Truncation | Active | [102] |
55 | Glu | Truncation | Active | [102] |
ID | Toxin | Species | Geographic Origin | Function | Ref |
---|---|---|---|---|---|
Pore-forming/hemolytic | |||||
- | Cytotoxin A-I a | Cerebratulus lacteus | Woods hole, MA, USA | Pore-forming; hemolytic | [5,104] |
- | Cytotoxin A-II a | Cerebratulus lacteus | Woods hole, MA, USA | Pore-forming; hemolytic | [5,104] |
P01527 | Cytotoxin A-III a | Cerebratulus lacteus | Woods hole, MA, USA | Pore-forming; hemolytic | [5,104] |
- | Cytotoxin A-IV a | Cerebratulus lacteus | Woods hole, MA, USA | Pore-forming; hemolytic | [104] |
6ENA b | Nemertide α-1 | Lineus longissimus | Koster Fiord, Swe | VGSC activator, paralytic | [120] |
- | Nemertide α-2 | Lineus longissimus | Koster Fiord, Swe | Likely VGSC activator, paralytic | [120] |
- | Nemertide β-1 | Lineus longissimus | Koster Fiord, Swe | Neurotoxin B-IV homolog. Likely paralytic. | [120] |
- | ”Nemertine” | Lineus ruber | Possible nemertide | [5] | |
- | ”Nemertine” | Tenuilineus bicolor f | Not stated | Possible nemertide | [5] |
- | ”Nemertine” | Lineus viridis | Not stated | Possible nemertide | [5] |
- | <5 kDa component | Lineus longissimus | Koster Fiord, Swe, and Millport Scot, UK | Paralytic. Likely α-nemertide | [25] |
- | Neurotoxin B-I c | Cerebratulus lacteus | Long Island Sound, NY, USA | Likely paralytic | [89] |
P01526 | Neurotoxin B-II c | Cerebratulus lacteus | Long Island Sound, NY, USA | Paralytic | [89] |
P01526 | Neurotoxin B-II | Cerebratulus lacteus | Woods hole, MA, USA | Paralytic | [104] |
- | Neurotoxin B-III c | Cerebratulus lacteus | Long Island Sound, NY, USA | Likely paralytic | [89] |
P01525 | Neurotoxin B-IV | Cerebratulus lacteus | Woods hole, MA, USA | Paralytic | [104] |
ID | Toxin Gene Homolog | Species | Geographic Origin | Proposed Function | Ref |
---|---|---|---|---|---|
Pore-forming/hemolytic | |||||
P01527 | Cytotoxin A-III | Cerebratulus marginatus | San Juan Island, WA, USA [130] | Pore-forming; hemolytic | [124] |
P01527 | Cytotoxin A-III | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Pore-forming; hemolytic | [124] |
P01527 | Cytotoxin A-III | Lineus longissimus | Erdeven + Roscoff, Fra [131] | Pore-forming; hemolytic | [124] |
P01527 | Cytotoxin A-III | Lineus ruber | Roscoff, Wimereux, Fra [131] | Pore-forming; hemolytic | [124] |
P01527 | Cytotoxin A-III | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Pore-forming; hemolytic | [15] |
Q54316 | Hemolysin B | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Hemolytic | [15] |
P54176 | Hemolysin-3 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Hemolytic | [15] |
A0A0N7HUN6 | Parborlysin-4 | Parborlasia corrugatus | Adelaide Island, Antarctica | Likely pore-forming, hemolytic | [119] |
A0A0P0CC97 | Parborlysin-5 | Parborlasia corrugatus | Adelaide Island, Antarctica | Likely pore-forming, hemolytic | [119] |
A0A0P0BUQ6 | Parborlysin-6 | Parborlasia corrugatus | Adelaide Island, Antarctica | Liekely pore-forming, hemolytic | [119] |
A0A0P0CHY3 | Parborlysin-7 | Parborlasia corrugatus | Adelaide Island, Antarctica | Likely pore-forming, hemolytic | [119] |
- | Parborlysin/cytotoxin homolog 1 (Locus_9778) | Cerebratulus marginatus | San Juan Island, WA, USA [124,130,132] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 2 ( Locus_9778) | Cerebratulus marginatus | San Juan Island, WA, USA [124,130,132] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 3 (Locus_40830) | Hubrechtella ijimai | Hamanko, Honshu, Jpn [132] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 4 (comp17199) | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 5 (comp55821) | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 6 (Contig1463) | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 7 (Comp16298) | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 8 (Comp9226) | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 9 (contig46055) | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 10 (Comp45258) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 11 (comp48) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 12 (comp21702) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 13 (contig49129) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 14 (comp17823/17-134) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 15 (contig31748) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 16 (comp17823/17-147) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 17 (comp17823/17-145) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 17 (contig56815) | Lineus longissimus | Koster Fiord, Swe | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 18 (comp52392) | Lineus ruber | Roscoff, Wimereux, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 19 (contig63996) | Lineus ruber | Roscoff, Wimereux, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 20 (contig3234) | Lineus ruber | Roscoff, Wimereux, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 21 (comp40150/seq2) | Lineus ruber | Roscoff, Wimereux, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 22 (comp40150/seq2) | Lineus ruber | Roscoff, Wimereux, Fra [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 23 (contig21527) | Lineus sanguineus | Not stated [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 24 (contig61445) | Lineus sanguineus | Not stated [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 25 (contig2073) | Ramphogordius pseudolacteus b | Not stated [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 26 (contig6541) | Ramphogordius pseudolacteus b | Not stated [131] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 27 (Locus_8475) | Riseriellus occultus | Liverpool, UK [132] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 28 (Locus_39410) | Riseriellus occultus | Liverpool, UK [132] | Likely pore-forming | [120] |
- | Parborlysin/cytotoxin homolog 29 (Locus_13571) | Riseriellus occultus | Liverpool, UK [132] | Likely pore-forming | [120] |
Q76CA2 | Echotoxin-2 | Cephalothrix hongkongiensis | Akkeshi, Hokkaido, Jpn [130] | Pore forming, hemolytic | [124] |
Q76CA2 | Echotoxin-2 | Cephalothrix linearis | Not stated | Pore forming, hemolytic | [124] |
Q76CA2 | Echotoxin-2 | Cerebratulus marginatus | San Juan Island, WA, USA [130] | Pore forming, hemolytic | [124] |
Q76CA2 | Echotoxin-2 | Lineus ruber | Roscoff, Wimereux, Fra [131] | Pore forming, hemolytic | [124] |
Q76CA2 | Echotoxin-2 | Tubulanus polymorphus | San Juan Island, WA, USA | Pore forming, hemolytic | [124] |
Q66SO3 | Galactose-specific lectin nattectin | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Ca2+-dependent hemagglutination activity | [15] |
A0ZSK3 | Neoverrucotoxin subunit alpha | Cerebratulus marginatus | San Juan Island, WA, USA [130] | SNTX/VTX toxin; hemolytic activity | [124] |
A0ZSK3 | Neoverrucotoxin subunit alpha | Paranemertes peregrina | San Juan Island, WA, USA | SNTX/VTX toxin; hemolytic activity | [124] |
A0ZSK4 | Neoverrucotoxin subunit beta c | Lineus longissimus | Erdeven + Roscoff, Fra [131] | SNTX/VTX toxin; hemolytic activity | [124] |
A0ZSK4 | Neoverrucotoxin subunit beta | Malacobdella grossa | Rhode Island, USA | SNTX/VTX toxin; hemolytic activity | [124] |
Q98989 | Stonustoxin | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | SNTX/VTX toxin; pore-forming, hemolytic | [124] |
Q98989 | Stonustoxin | Lineus ruber | Roscoff, Wimereux, Fra [131] | SNTX/VTX toxin; pore-forming, hemolytic | [124] |
Q91453 | Stonustoxin subunit beta | Tubulanus polymorphus | San Juan Island, WA, USA | SNTX/VTX toxin; pore-forming, hemolytic | [124] |
P58912 | Toxin PsTX-60B | Cephalothrix hongkongiensis | Akkeshi, Hokkaido, Jpn [130] | MACPF toxin domain; hemolytic | [124] |
P58912 | Toxin PsTX-60B | Cephalothrix linearis | Not stated | MACPF toxin domain; hemolytic | [124] |
Q76DT2 | Toxin AvTX-60A | Cephalothrix linearis | Not stated | MACPF toxin domain; hemolytic | [124] |
Neurotoxins/Acting on ion-channels | |||||
Q92035 | Acetylcholinesterase | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Synaptic cleft hydrolysis of acetylcholine | [15] |
P05486 | Conophysin-conopressin | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Targets vasopressin-oxytocin related receptors | [15] |
6ENA d | Nemertide α-1 | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | VGSC activator, paralytic | [120] |
6ENA d | Nemertide α-1 | Lineus longissimus | Koster Fiord, Swe | VGSC activator, paralytic | [120] |
6ENA d | Nemertide α-1 | Lineus ruber | Roscoff, Wimereux, Fra [131] | VGSC activator, paralytic | [120] |
- | Nemertide α-2 | Lineus longissimus | Koster Fiord, Swe | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-2 | Lineus ruber | Roscoff, Wimereux, Fra [131] | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-3 | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-3 | Ramphogordius pseudolacteus b | Not stated [131] | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-4 | Lineus sanguineus | Not stated [131] | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-5 | Ramphogordius pseudolacteus b | Not stated [131] | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-6 | Lineus sanguineus | Not stated [131] | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-7 | Lineus ruber | Roscoff, Wimereux, Fra [131] | Likely VGSC activator, paralytic | [120] |
- | Nemertide α-8 | Riseriellus occultus | Liverpool, UK [132] | Likely VGSC activator, paralytic; incomplete sequence | [120] |
- | Nemertide β-1 | Lineus longissimus | Koster Fiord, Swe | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-1 | Lineus ruber | Roscoff, Wimereux, Fra [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-2 | Lineus longissimus | Koster Fiord, Swe | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-2 | Lineus ruber | Roscoff, Wimereux, Fra [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-3 | Lineus longissimus | Koster Fiord, Swe | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-4 | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-5 | Ramphogordius pseudolacteus b | Not stated [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-6 | Ramphogordius pseudolacteus b | Not stated [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-7 | Lineus ruber | Roscoff, Wimereux, Fra [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-8 | Lineus sanguineus | Not stated [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
- | Nemertide β-9 | Lineus sanguineus | Not stated [131] | Neurotoxin B-IV homolog, likely paralytic | [120] |
Q09GJ9 | Cysteine-rich venom protein | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Ca2+-channel impairment; paralytic | [15] |
Q3SB03 | Cysteine-rich venom protein pseudechetoxin-like | Malacobdella grossa | Rhode Island, USA | Possible Shk-toxin | [124] |
Q3SB03 | Cysteine-rich venom protein pseudechetoxin-like | Paranemertes peregrina | San Juan Island, WA, USA | Possible Shk-toxin | [124] |
Q3SB05 | Cys-rich venom protein pseudechetoxin-like | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Possible Shk-toxin | [15] |
P69929 | Delta-actitoxin-Amc1a | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | May inhibit VGSC | [15] |
D2Y1Y2 | Mu-theraphotoxin-Hhn2a 4 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Blocks TTX-sensitive VGSC | [15] |
P0C8G6 | Perivitellin-2 67 kDa subunit | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Neurotoxin present in eggs, acts on enterocytes | [15] |
P0DKT2 | Turripeptide Gsg9.2 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Ion-channel inhibitor | [15] |
Coagulation | |||||
Q7T3S7 | Acidic phospholipase A2 EC-I | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Inhibits platelet aggregation | [15] |
Q3C2C1 | Phospholipase A2 AP-PLA2-II | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Capillary permeability-increasing and hemorrhagic activities | [15] |
Q0ZZJ6 | A. superbus venom factor 1 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Complement-activating | [15] |
P0CH47 | Probable phospholipase A1 magnifin | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Causes platelet aggreagation, phospholipase activity | [15] |
E0Y418 | Serine protease VLSP-1 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | May act in prey hemostasis system | [15] |
Q6X5S5 | Snaclec 27 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Interferes with platelet aggregation | [15] |
Q9DEA1 | Snaclec agkicetin-C subunit beta | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Antithrombotic action | [15] |
P0C929 | Snaclec bothroinsularin subunit alpha | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Inhibits platelet aggregation | [15] |
I7ICN3 | Snaclec bothroinsularin subunit beta | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Integrin antagonist | [15] |
Q38L02 | Snaclec dabocetin subunit alpha | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Inhibits platelet aggregation | [15] |
Q58L91 | Venom prothrombin activator oscutarin-C non-catalytic subunit | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Prothrombin activator; attacks hemostatic system | [15] |
J3SBP3 | Venom phosphodiesterase 2 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Nuclease activity and platelet aggregator | [15] |
Other proposed activities | |||||
A0FKN6 | Astacin-like metalloprotease toxin 1 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Degrades fibronectin, fibrinogen and gelatin in vitro | [15] |
P0DN10 | U-actitoxin-Avd3i | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Serine protease inhibitor of kallikreins | [15] |
P81382 | L-amino acid oxidase | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Oxidative deamination of hydrophobic and aromatic residues | [15] |
B2DCR8 | SE-cephalotoxin | Cephalothrix linearis | Not stated | Toxic function unknown | [124] |
B2DCR8 | SE-cephalotoxin | Cerebratulus marginatus | San Juan Island, WA, USA [130] | Toxic function unknown | [124] |
B2DCR8 | SE-cephalotoxin | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Toxic function unknown | [124] |
B2DCR8 | SE-cephalotoxin | Lineus longissimus | Erdeven + Roscoff, Fra [131] | Toxic function unknown | [124] |
B2DCR8 | SE-cephalotoxin | Lineus ruber | Roscoff, Wimereux, Fra [131] | Toxic function unknown | [124] |
P0A968 | Cold shock-like protein CspD | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Inhibitor of DNA replication | [15] |
P26831 | Hyaluronoglycosaminidase | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Likely to act on connective tissue | [15] |
P00984 | Kunitz-type serine protease inhibitor dendrotoxin E | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Inhibitor of trypsin and chymotrypsin | [15] |
Q9KS12 | Multifunctional-autoprocessing repeats-in-toxin | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Destroys actin cytoskeleton | [15] |
Q66S25 | Natterin-1 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Edema and nociception | [15] |
Q66S13 | Natterin-4 | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Edema and nociception | [124] |
Q66S13 | Natterin-4 | Tubulanus polymorphus | San Juan Island, WA, USA | Edema and nociception | [124] |
Q66S13 | Natterin-4 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Edema and nociception | [15] |
- | Natterin-4 homolog (Cm6) | Cerebratulus marginatus | San Juan Island, WA, USA [130] | Inferred from reciprocal BLAST, likely edema and nociception | [124] |
K7Z9Q9 | Nematocyst expressed protein 6 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Metalloendopeptidase activity | [15] |
A4USB4 | Phospholipase D LiSicTox-AlphaVI | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Hydrolysis of sphingomyelin; causes dermonecrosis and inflammation | [15] |
Q1W694 | Phosopholipase D LiSicTox-betaID1 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Hydrolysis of sphingomyelin; causes dermonecrosis and inflammation | [15] |
Q75WF2 | Plancitoxin-1 | Cephalothrix hongkongiensis | Akkeshi, Hokkaido, Jpn [130] | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Hepatotoxin | [15] |
Q75WF2 | Plancitoxin-1 | Cephalothrix linearis | Not stated | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Cerebratulus marginatus | San Juan Island, WA, USA [130] | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Lineus lacteus a | Banyuls, Fréjus, Fra [131] | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Lineus longissimus | Erdeven + Roscoff, Fra [131] | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Lineus ruber | Roscoff, Bretagne, Wimereux, France [131] | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Malacobdella grossa | Rhode Island, USA | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Paranemertes peregrina | San Juan Island, WA, USA | Hepatotoxin | [124] |
Q75WF2 | Plancitoxin-1 | Tubulanus polymorphus | San Juan Island, WA, USA | Hepatotoxin | [124] |
C1IC50 | Protease inhibitor-1 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Serine protease inhibitor | [15] |
A8YPR9 | Snake venom metalloprotease inhibitor 02A10 | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Metalloproteinase inhibitor during glandular storage | [15] |
P86548 | Soybean toxin 17 kDa chain | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Involved in plant defense | [15] |
B5U2W0 | Venom serine protease Bi-VSP | Notospermus geniculatus | Ushimado Mar Inst Okayama Univ, Jpn | Serine protease, induces melanization in target insects | [15] |
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Göransson, U.; Jacobsson, E.; Strand, M.; Andersson, H.S. The Toxins of Nemertean Worms. Toxins 2019, 11, 120. https://doi.org/10.3390/toxins11020120
Göransson U, Jacobsson E, Strand M, Andersson HS. The Toxins of Nemertean Worms. Toxins. 2019; 11(2):120. https://doi.org/10.3390/toxins11020120
Chicago/Turabian StyleGöransson, Ulf, Erik Jacobsson, Malin Strand, and Håkan S. Andersson. 2019. "The Toxins of Nemertean Worms" Toxins 11, no. 2: 120. https://doi.org/10.3390/toxins11020120