Table 6.
Overview of putative toxin gene sequences found in nemerteans.
| 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] |
ID is short for UniProtKB entry (uniprot.org). The proposed functions listed are the result of automatic annotation, extracted from uniprot.org entries, or for sequences lacking uniprot entry, inferred from activities of known homologs by the authors of this review. a In source also referred to as Ramphogordius lacteus (synonymous). b In source referred to as Lineus pseudolacteus (synonymous). c In source assigned as subunit alpha. d PDB code. Species are denoted according to WoRMS, World Register of Marine Species as of 19-02-11 [54].