Biological Activity of Recently Discovered Halogenated Marine Natural Products

Abstract

This review presents the biological activity-antibacterial, antifungal, anti-parasitic, antiviral, antitumor, antiinflammatory, antioxidant, and enzymatic activity-of halogenated marine natural products discovered in the past five years. Newly discovered examples that do not report biological activity are not included.

Keywords: antibacterial; antiinflammatory; antioxidant; antiparasitic; antitumor; antiviral; natural products; organobromine; organochlorine; organohalogen.

Figure 1

Structures of gemmacolide briarane diterpenoids from Dichotella gemmacea [30,31].

Figure 1

Structures of gemmacolide briarane diterpenoids from Dichotella gemmacea [30,31].

Figure 2

Structures of selected dichotellide briarane diterpenoids from Dichotella gemmacea [34].

Figure 3

Structures of fragilisinins A–L briarane diterpenoids from Junceella fragilis [35].

Figure 3

Structures of fragilisinins A–L briarane diterpenoids from Junceella fragilis [35].

Figure 4

Structures of selected sinulariol cembrane diterpenoids from Sinularia rigida [36].

Figure 5

Structures of cochliomycins A–C (39–41) from Cochliobolus lunatus [37,38].

Figure 6

Structures of (±)-pestalachlorides D (42) and C (43) from Pestalotiopsis sp. [39,40].

Figure 7

Structures of alcyopterosins 44 and 45 from Alcyonium roseum [41], and strepchloritides A (46) and B (47) from Streptomyces sp. OUCMDZ-1703 [42].

Figure 8

Brominated compounds 48–50 from Paramuricea clavata [43].

Figure 9

Structures of pseudoceramines A–D (51–54) from the sponge Pseudoceratina sp. [44].

Figure 10

Structures of bromotyrosines 55–58 from the sponge Pseudoceratina sp. [45].

Figure 11

Structures of purpuroines A–J (59–68) from the sponge Iotrochota purpurea [46].

Figure 12

Structures of massadines 69–71 from the sponge Axinella sp. [47].

Figure 13

Structures of indolo[3,2-a]carbazoles 72 and 73 from the sponge Asteropus sp. [48].

Figure 14

Structures of dictyodendrins F–J (74–78) from the sponge Ianthella sp. [49].

Figure 15

Structures of nakijinamines 79–84 and 6-bromoconicamin (85) from the sponge Suberites sp. [50].

Figure 16

Structures of agelasines O–U (86–92) from the sponge Agelas sp. [52].

Figure 16

Structures of agelasines O–U (86–92) from the sponge Agelas sp. [52].

Figure 17

Structures of bromopyrroles 93–99 from the sponge Agelas sp. (SS-162) [53,54].

Figure 17

Structures of bromopyrroles 93–99 from the sponge Agelas sp. (SS-162) [53,54].

Figure 18

Structures of kalihinols M–T (100–107) from the sponge Acanthella caverenosa [55].

Figure 19

Structures of red algae metabolites 108–114 [58,59,60].

Figure 20

Structures of omaezallenes 115–117 from the red alga Laurencia sp. [61].

Figure 21

Structures of bromoindoles 118–121 and bromosphaerols 122–126 [62,63].

Figure 22

Structures of bromophycoic acids A–E (127–131) from the red alga Callophycus sp. [64].

Figure 23

Structures of eudistomins Y₂–Y₇ (132–137) from the ascidian Synoicum sp. [65].

Figure 24

Structures of the cadiolides, synoilides, and rubrolides (138–151) from the ascidians Synoicum and Pseudodistoma antinboja [67,68].

Figure 25

Structures of rubrolides 152–157 from the ascidian Synoicum globosum [69].

Figure 26

Structures of synoxazolidinones A (158) and C (159), and pulmonarians A (160) and B (161) from the ascidian Synoicum pulmonaria [70].

Figure 27

Structures of fungal metabolites 162–164 from the fungus Bartalinia robillardoides strain LF550 [71].

Figure 28

Structures of spiromastixones A–O (165–179) from the fungus Spiromastix sp. [72].

Figure 29

Structures of merochlorins A–D (180–183) from Streptomyces sp. CNH-189 [73,74].

Figure 30

Structures of napyradiomycins A–F (184–189) from Streptomyces CNQ-329 and CNH-070 [75].

Figure 31

Structures of napyradiomycins 191–193 [76].

Figure 32

Structure of salimabromide (194) from the marine myxobacterium Enhygromxya salina [77].

Figure 33

Structures of honaucins A–C (195–197) from the cyanobacterium Leptolyngbya crossbyana [78], and pitinoic acids A–C (198–200) from a cyanobacterium [79].

Figure 34

Structure of aurantoside K (201) from the sponge Melophlus sp. [80] and aurantoside J (202) from the sponge Theonella swinhoei [81].

Figure 35

Structure of theonellamide G (203) from the sponge Theonella swinhoei [82].

Figure 36

Structures of hamigerans 204–211 from the sponge Hamigera tarangaensis [83].

Figure 37

Structures of agelamadins C–E (212–214) from the sponge Agelas sp. SS-162 [84].

Figure 38

Structures of nagelamides U–Z (216–221) and 222–224 from Agelas spp. sponges [85,86,87].

Figure 39

Structures of laurecomins A–D (225–228) from the red alga Laurencia composita [88].

Figure 40

Structures of brominated sesquiterpenes 229–234 from the red alga Laurencia okamurai [89].

Figure 41

Structures of symphyocladins A–G (236–242) and other bromophenols from the red alga Symphyocladia latiuscula [90,91,92].

Figure 42

Structure of 2,4,7-tribromotryptamine (246) from the bryozoan Chartella membranaceatruncata [93].

Figure 43

Structure of forazoline A (247) from Actinomadura sp. [94].

Figure 44

Structures of balticidins A–D (248–251) from the cyanobacterium Anabaena cylindrica Bio33 [97,98].

Figure 44

Structures of balticidins A–D (248–251) from the cyanobacterium Anabaena cylindrica Bio33 [97,98].

Figure 45

Structures of psammaplysins H (252), G (253), and F (254) from the sponge Pseudoceratina sp. [104].

Figure 46

Structures of psammaplysins 255–275 from the sponge Aplysinella strongylata [105].

Figure 46

Structures of psammaplysins 255–275 from the sponge Aplysinella strongylata [105].

Figure 47

Structures of araplysillins 276–280 from the sponge Suberea ianthelliformis [106].

Figure 48

Structures of iotrochamides A (281) and B (282) from the sponge Iotrochota sp. [108].

Figure 49

Structure of tsitsikammamine C (283) from the sponge Zyzzya sp. [109].

Figure 50

Structures of manadoperoxides E–K (284–290) and peroxyplakoric ester C (291) from the sponge Plakortis cfr. lita [110].

Figure 51

Structures of 292 and opacalines A–C (293–295) from the ascidian Pseudodistoma opacum [112].

Figure 52

Structure of kororamide A (296) from the bryozoan Amathia tortuosa [113].

Figure 53

Structures of coibacins A–D (297–300) from the cyanobacterium Oscillatoria sp. [114].

Figure 54

Structures of radicicols B–D (301–303) from Humicola fuscoatra [119].

Figure 55

Structures of emerimidines A (304) and B (305), and emeriphenolicins A–D (306–309) [121].

Figure 56

Structures of 310–313 from the ascidian Synoicum sp. [122].

Figure 57

Structures of aplysiatoxins 314 and 315 from the cyanobacterium Trichodesmium erythraeum [123].

Figure 58

Structures of lanosol (316) and 317 from the red alga Neorhodomela aculeata [124] and peyssonol A (318) and synthetic analogues 319–321 [125].

Figure 59

Structures of 322 and 323 from the sponge Penares sp. [126].

Figure 60

Structures of PM050489 (324) and PM060184 (325) from the sponge Lithoplocamia lithistoides [127].

Figure 61

Structure of phorbaketal N (326) from the sponge Phorbas sp. [128].

Figure 62

Structures of psammaplysins 327–330 and ceratinamines 331–334 from the Suberea sp. sponge [129].

Figure 63

Structures of brominated acetylenes 335 and 336 from the Haliclona sp. sponge [130].

Figure 64

Structure of callyspongiolide (337) from the sponge Callyspongia sp. [131].

Figure 65

Structures of phormidolides B (338) and C (339) from a sponge of the Petrosiidae family [132].

Figure 66

Structure of mollenyne (340) from the sponge Spirastrella mollis [133].

Figure 67

Structure of bromotheoynic acid (341) from the sponge Theonella swinhoei [134].

Figure 68

Structures of brominated alkaloids 342–353 from the sponge Stylissa sp. [135].

Figure 69

Structures of 6′-iodoaureol (354), aureol (360), and indoles 355–362 from the sponge Smenospongia sp. [136].

Figure 70

Structures of smenamides A (363) and B (364), and smenothiazoles A (365) and B (366) from the sponge Smenospongia aurea [137,138].

Figure 71

Structure of sesquibastadin 1 (367) from the sponge Ianthella basta [139].

Figure 72

Structures of ceratinines A–E (368–372) and subereamolline A (373) from the sponge Pseudoceratina arabica [140].

Figure 73

Structures of pseudoceralidinone A (374) and aplysamine 7 (375) from Pseudoceratina verrucosa [141].

Figure 74

Structures of cavernenes A–D (376–379), kalihinenes E (380) and F (381) and kalipyran C (382) from the sponge Acantella cavernosa [142].

Figure 75

Structures of similisines A (383a) and B (383b), and oxindole 384 from Laurencia similis [151].

Figure 76

Structures of polycyclic triterpenoids 385–391 from Laurencia viridis [152,153,154].

Figure 77

Structures of halogenated monoterpenes from Plocamium suhrii [156].

Figure 78

Structure of synoxazolidinone (399) from the ascidian Synoicum pulmonaria [157].

Figure 79

Structures of tanjungides A (400) and B (401) from the tunicate Diazona cf formosa [158].

Figure 80

Structures of didemnins 402–405 from the tunicate Trididemnum solidum [159].

Figure 81

Structures of klymollins I–S (406–416) from the soft coral Klyxum molle [160].

Figure 82

Structures of gemmacolides AA–AR (417–434) from the gorgonian Dichotella gemmacea [161].

Figure 83

Structures of greensporones 435–448 from the freshwater aquatic fungus Halenospora sp. [162].

Figure 84

Structures of benzophenones 449–452 and xanthone 453 from Stachybotry sp. HH1 ZDDS1F1-2 [163].

Figure 85

Structures of 454–456 from the fungus Nigrospora sp. MA75 [164].

Figure 86

Structures of chlorinated averantin anthraquinones 457–463 from the fungus Aspergillus sp. SCS10 FO63 [165].

Figure 87

Structure of dankastatin C (464) from the fungus Gymnascella dankaliensis [166].

Figure 88

Structures of polyporapyranones A–H (465–472) from the fungi Polyporales PSU-ES44 and PSU-ES83 [167].

Figure 89

Structures of chaetomugilins S, T, and U (473–475) from the fungus Chaetomium globosum [168].

Figure 90

Structures of isochromophilones X–XII (476–478) from the fungus Diaporthe sp. [169].

Figure 91

Structures of ligerin (479) and 480–483 from the fungi Penicillium spp. [170,171].

Figure 92

Structures of carbamidocyclophanes F (484) and G (485) from the cyanobacterium Nostoc sp., and fischerindoles 486–489 from the cyanobacterium Fischerella sp. [172,173].

Figure 93

Structures of isomalyngamides A (490) and A-1 (491) from the cyanobacterium Lyngbya majuscule [174].

Figure 94

Structures of malyngamides 2 (492) from Lyngbya sordida and 4 (493) from Moorea producens [175,176].

Figure 95

Structures of lyngbyabellins 494–498 from the cyanobacterium Moorea bouillonii [177].

Figure 96

Structures of Streptomyces sp. ammosamide D (499) and chlorizidine A (500) [178,179].

Figure 97

Structures of spiroindimicins A–D (501–504) and indimicins A–E (505–509) and lynamicins F (510) and G (511) from Streptomyces sp. SCS10 03032 [180,181].

Figure 98

Structures of napyradiomycins 512–515 from actinomycete strain CNQ525 [182].

Figure 99

Structures of ammonificins C (516) and D (517) from Thermovibrio ammonificans [183].

Figure 100

Structures of aspidostomides A–H (518–525) and aspidazide A (526) from the bryozoan Aspidostoma giganteum [184].

Figure 101

Structures of phorbazoles 527 and 528 from the nudibranch Aldisa andersoni [185].

Figure 102

Structures of palmadorins (529–535) from the nudibranch Austrodoris kerguelenensis [186].

Figure 103

Structures of oculiferane (536) and epi-obtusane (537) from the sea hare Aplysia oculifera [190].

Figure 104

Structures of bromophenols 538–545 from the alga Rhodomela confervoides [191].

Figure 105

Structures of bromocatechols 546–551 from the alga Rhodomela confervoides [192].

Figure 106

Structures of bromocatechols 552–556 from the red algae Symphyocladia latiuscula and Vertebrata lanosa [193,194].

Figure 107

Structures of 558–560 from the sponges Hyrtios sp. and Zyzza fuliginosa [195,196].

Figure 108

Structures of iodinated acetylenic acids 561–564 from the sponges Suberites mammilaris and S. japonicus [197].

Figure 109

Structures of herdmanines A–D (565–568) from the ascidian Herdmania momus [198].

Figure 110

Structures of frajunolides L–S (569–576) from the gorgonian Junceella fragilis [199,200].

Figure 111

Structures of juncenolides M–O (577–579) from the gorgonian Junceella juncea [201].

Figure 112

Structures of phenazines (581–584) from Streptomyces sp. CNS284 [203,204].

Figure 113

Structures of dispacamide E (585) and pyrrole 586 from the sponges Stylissa massa and Stylissa flabelliformis [207].

Figure 114

Structures of polybromides 587–591 from the red alga Laurencia similis [208].

Figure 115

Structures of pulmonarins A (592) and B (593) from the ascidian Synoicum pulmonaria [209] and mutafuran H (594) from the sponge Xestospongia testudinaria [210].

Figure 116

Structures of aeruginosins 595–604 from the cyanobacteria Microcystis aeruginosa and Microcystis spp. [211,212,213].

Figure 117

Structures of bromotyrosines 605–611 from the sponges Aplysinella sp. and Callyspongia sp. [214,215].

Figure 118

Structures of bromo carboxylic acids 612–616 from the sponge Xestospongia testudinaria [216].

Figure 119

Structures of herdmanines E–K (617–623) from the ascidian Herdmania momus [217].

Figure 120

Structures of placotylenes A (624) and B (625) from the sponge Placospongia sp. [218] and chalinulasterol (626) from the sponge Chalinula molitba [219].

Figure 121

Structures of janthielamide A (628), kimbeamides A–C (629–631), and kimbelactone A (632) from cyanobacteria [220].

Figure 122

Structures of malbrancheamides 633–636 from the fungus Malbranchea aurantiaca [221].

Figure 123

Structures of okamurene E (637) and okamuragenin (638) from the red alga Laurencia okamurai, and 7-hydroxylaurene (639) [222].

Figure 124

Structures of mycotoxins 640–643 from the fungus Aspergillus sp. SCSGAF0093 [223].