n 1968, Fowden wrote that present information As shown in Table 1, the number of known natural

suggests that organic compounds containing co- organohalogens has increased dramatically since 1968,
valently bound halogens are found only infre- and the current number of identified compounds
quently in living organisms ( I ) . Although this stands at about 2000 (5). Consequently, this review pro-
observation was undeniable 25 years ago, it is vides a very limited glimpse of this fascinating field of
nothing but a myth today. natural products.
chlorinated Occurrence
and other halo- Simple alkanes and
genated chemi- related compounds.
cals are dis- The simplest natural
charged into organohalogen com-
our biosphere by pounds-halogenated
plants, marine organ- alkanes-are abundant
isms, insects, bacte- on our planet (Table 2 ) .
ria, fungi, and mam- Chloromethane is pro-
mals, and by other duced by marine algae
natural processes. En- (101, giant kelp ( I f ) ,
zymatic, thermal, and wood-rotting fungus
other natural pro- (12). the ice plant ( l o ) ,
cesses are constantly cultivated mushrooms
occurring in t h e (131, the pencil cedar
oceans, in the atmos- 1141, the evergreen cy-
phere, and in the soil press ( 1 4 ) , several
that lead to the forma- Fomes fungi (15), and
tion of chlorinated phytoplankton (16).
phenols and myriad Chloride ion is nor-
other chlorinated mally present in plants,
chemicals, including wood, soil, and miner-
dioxins a n d CFCs, als (12, 141, and their
that previously were combustion inevitably
thought to result only leads to the formation
from the actions of of organochlorine com-
humans. It is clear pounds. Consequently,
that these natural pro- forest fires ( 1 7);brush
cesses have been pro- and vegetation burning
ducing chlorinated ( I 8);and volcanoes ( 14,
compounds and have 19, 201, including the
been a vital compo- eruptions of Mt. St.
nent of our ecosystem Helens ( 2 2 ) and
for eons. Kilauea (221, all pro-
Chlorine is in the
political and environ- -
duce sienificant and. in
some cases, massive
mental spotlight (21, quantities of chloro-
a n d a n aggressive methane. This global
campaign by the envi- emission rate of chloro-
ronmental organiza-
tion Greenpeace to
ban summarily a l l
production and uses
- methane from the ma-
rine and terrestrial bio-
mass is 5 million tons
per year (23),whereas
of chlorine (and bro- anthropogenic chloro-
methane emissions are
only 26,000 tons per
year (12). Several other
s i m p l e haloalkanes
and the first Interna- also have natural
tional Conference on sources (Table 2).
Naturally Produced GCD?ON W. GRIBBLE In addition to the
Organohalogens was Iartn b College, Hanovel; N H 037 simple one- and two-
held last year in The carbon halogens (Table
Netherlands (3). Not I 21, numerous haloge-
only are naturally oc- nated alcohols, ketones,
curring organohalogen compounds ubiquitous in our carboxylic acids and amides, aldehydes, epoxides, and
environment, but concentrations of some of these alkenes have also been isolated and characterized from
chemicals exceed their anthropogenic levels. Although marine algae (24-26).Indeed, nearly 100 different chlo-
myriad examples of chlorine-, bromine-, iodine-, and rinated, brominated, and iodinated compounds have
even several fluorine-containing natural products exist been found in Asparagopsis taxiformis, the favorite ed-
(41, the present review focuses principally on organo- ible seaweed of most Hawaiians (24).The following are
chlorine compounds. samples of those chlorinated compounds (p. 312A):

310 A Envimn. Sci. Technol.. VoI. 28. No. 7. 1994 0013-936X/94/0927-31OA$04.50/00 1994 American Chemical Society
 0 CI
cgc K CCI3 Br
Br+Br
The simple marine haloalkanes,
such as chloroform and bromoform,
could arise from in vivo haloform
reactions, a mechanism that may
enable algae, for example, to secrete
continuously these antipredator
chemicals (24,271.
Volcanoes produce large quanti-
ties of both hydrogen chloride (up
to 3 million tons per year) and hy-
drogen fluoride (up to 11 million
eel
0
i 0
312A Environ. W.Technol.. Vol. 28. No. 7 , l m
tons per year) (14, 28). It has been
proposed that HCI and HF can react
with organic compounds to pro-
duce organohalogens ( 2 8 ) . Al-
though the quantities may be small
compared with anthropogenic lev-
els, several chlorofluorocarbons
(CFCs) have been detected in volca-
nic gases from the Santiaguito vol-
cano in Guatemala ( 1 9 )and the Kam-
chatka volcanoes in Siberia ( 1 4 ) . It
is estimated that 75% of the worlds
500-700 active volcanoes are capa-
ble of producing CFCs ( 1 4 ) . The
CFCs and compounds below show
the organochlorines produced by
these volcanoes.
CFC1, (Freon 11) CF,C1, (Freon 12)
CHF,Cl CHFCl,
5 uwow are identified by number in the text)
OH
ci%r
2 3 -Cl
CH,Cl, CH,CCI,
F,C=CF, FClCkCF,
CCl,FCClF, (Freon 113)
Cl,C=CCl, CI,C=CHCl
The concentrations of these chemi-
cals as measured in and around the
solfataric vents of the Kamchatka
volcanoes range from 0.4 ppb to
160 ppb of CFCs. Deep drill wells
(one mile or deeper) are also a
source of several organochlorine
compounds and CFCs ( 1 4 ) .
Terpenes a n d related com-
pounds. Terpenes are ubiquitous in
terrestrial organisms and are essen-
tial for life, but marine terpenes
were not discovered until 1955,and
halogenated marine terpenes were
lac
CI )i+$cl
4 cI 5:(telfairine)
Br
first isolated only in 1963 (2931).
Examples of chlorinated terrestrial
terpenes were first reported in 1969
(32).Since then, there has been a
veritable explosion of activity, and
a legion of new chlorinated and bro-
minated terpenes has been isolated
and identified (30,31,33,34).Nota-
bly, the red algae Laurencia and
Plocamium have provided a rich
and diverse assortment of chlori-
nated and brominated terpenes over
the past 25 years (structures 1-6).
Nearly 20 chlorinated diterpenes
and one tetraterpene have been iso-
lated from several soft corals (35-
39). An example of the structural
complexity of these compounds is
erythrolide C (Structure 7) (38).
Another very large group of halo-
genated organic compounds is the
nonterpenes, compounds that do
not arise from an obvious terpenoid
pathway. The Guam bubble shell
(Haminoea cymbalum) contains
kumepaloxane (Structure 8 ) (40). a
feeding-deterrent chemical that is
discharged when this mollusk is
disturbed by unwelcome carnivo-
rous fishes. Marine red algae, espe-
cially Laurencia, are a source of fan-
tastically complex nonterpenoid
chemicals. Thus, L. implicata has
yielded six new cyclic ethers, some
of which are allenes (e.g., Structure
9) (41, 42). Nostoc blue-green algae
are recognized as a threat to human
health when they infest drinking-
water sources (43. 44). Cultivation
and extraction of Nostoc linckia
have yielded four unusual chlori-
nated paracyclophanes. for exam-
Environ. Sd. Technol., VoI. 28. No. 7, 1994 3131
ple, nostocyclophane D (Structure
10)(451.
Amino acids and peptides. With
the exception of the naturally oc-
curring iodinated tyrosines such as
thyroxine, there are relatively few
examples of halogenated amino ac-
ids and simple peptides. The ma-
rine sponge Dysidea herbacea con-
tains four novel trichloromethyl
metabolites, including dysidin
[ S t r u c t u r e 11) a n d d y s i d e n i n
[Structure 12) (46-50). Several
Streptomyces and Pseudomonas
spp. contain chlorinated amino
acids and/or peptides, many of
which have potent antibacterial
activity. For example, Streptomy-
ces griseosporeus produces y-chlo-
ronorvaline (Structure 13) ( 5 1 ) ,
a n d Streptomyces viridogenes

he number of naturally occurring organohalogen compounds
!ar Reviewer summary
~.
168 Fowden 30 organochlorine natural products and
a lew containing bromine, iodine. and
fluorine
70 fungal metabolites containing
chlorine
200 organohalogen cornpounds from a
sources (150 organochlorine, 50
organobromine)
80 new fungal metabolites containing
chlorine
130 organochlorines from higher plants
61 1 new organohalogen compounds
from all sources isolated between 1980
and 1991
yields Structure 14 (52). Egregio menziesii produces three
Alkaloids. Although terrestrial prostaglandin-like chlorinated oxy-
plant alkaloids have been scruti- lipins, for example, egregiachloride
nized by chemists for more than a A (Structure 19) ( 6 4 ) . Of some 22
century, very few of these nitrogen freshwater algae species that were
compounds contain halogen of any examined for chlorosulfolipids, all
kind. Recently, oxypterine [Struc- but one contained quantities of
ture 151, a dichlorinated pyrroliz- these novel lipids (65, 66).
idine derivative, was found to be Pyrroles. The pronounced reac-
present in the herb Lotononis tivity of pyrroles in electrophilic
oxyptero (53),and a Streptomyces substitution reactions endorses the
sp. produces clazamycin A (Struc- observation that chlorinated and
ture 16) and B (54-56). brominated pyrroles are found
Steroids. Steroids rarely contain widely in nature. Following the iso-
halogen. However, a few examples lation in 1958 of pyoluteorin (Struc-
of chlorinated steroids are found in ture 201, a new antibiotic from
the plants Withonio somnifera, Ac- Pseudomonas oeruginoso (67), nu-
nistus breviflorus, Phvsolis peruvi- merous additional natural chlori-
onu. and johoroso moyelionico. nated and brominated pyrroles have
such a5 iaborochlorodiol IStruclure been disi:ovcrorl. 'I'hc soil niicrobe
17) (57).'The first three examples of Streptomyces sp. produces pyrrolo-
chlorinated marine steroids-kihe- mycin B (Structure 21) (68),and a
isterones C, D, and E-were re- soil Streptomyces sp. produces the
cently characterized from the Maui novel neopyrrolomycin (Structure
sponge Strongylacidon sp. (58). 221, a metabolite that has biphenyl-
Fatty acids, prostaglandins, and type optical activity (69). Many of
lipids. Although fluoroacetic acid the pyrrolomycins have strong anti-
and fluoro-fatty acids in certain ter- biotic activity, and a clinical drug
restrial plants have been known for from this structural type seems to be
many years (59, 60),chloro-fatty ac- a real possibility.
ids were unknown until recently. Indoles. The indole ring system
The edible jellyfish and the white has the distinction of being embod-
sea jellyfish (Auritio ourito) contain ied in the indigo derivative Tyrian
six fatty acid chlorohydrins (61). purple, the ancient Egyptian dye ex-
Mammalian prostaglandins are of tracted from mollusk shells and the
paramount importance in the regu- focus of a significant industry in
lation of physiological processes. Mediterranean countries (70). The
Therefore, it was of enormous inter- marine acorn worm Ptychodero
est when chlorinated prostaglan- Povo loysanica produces the unsta-
dins were discovered in the octo- ble 3-chloroindole (Structure 23)
coral Telesto riisei (62) and in the and 3-chloro-6-bromoindole com-
stolonifer Clavuloria viridis (63), a pounds that are responsible for the
marine animal. A total of eight peculiar "iodoform-like" odor of
novel chlorinated prostaglandins this animal (71).The 4-chloroindole
have been identified [e.g., puna- ester (Structure 24) and the corre-
glandin 1 (Structure 18)) (62),some sponding carboxylic acid are found
of which have potent antitumor ac- in Pisum sativum and several other
tivity (63). The marine brown alga terrestrial plants (lentil, sweet pea,
314A Environ. Sci. Technol., Vol. 28, No. 7, 1994
sea pea, vetch) (72, 73). Like 3-in-
doleacetic acid, these compounds
function as very strong plant growth
hormones. A blue-green alga, Hapo-
losiphon fontinolis, contains 12
chlorinated isonitriles, one of
which is hapalindole A (Structure
25) (74).
The deep water Bahamas sponge
Botzello sp. produces six chlori-
nated indoles, e.g., batzelline A
(Structure 26) ( 7 5 ) ,and nature's vir-
tuosity in organic synthesis is fur-
ther revealed by the marine hryo-
zoan Chartello popyroceo, which
constructs a complement of five ha-
logenated indoles, such as chartel-
line A (Structure 27) (76-78).
Miscellaneous heterocycles. Some
interesting halogenated thiophenes
are found in certain plants. For ex-
ample, Pterocaulon virgatum con-
tains five chlorinated thiophenes
(79, and six species of Echinops are
found to contain Structure 28 (80).
Only a few examples of nucleic acid
bases are known to contain halogen.
An Actinomyces sp. produces 2 ' -
chloropentostatin (Structure 291
181, 82).The first example of a chlo-
rinated porphyrin was recently iso-
lated in trace quantities from cul-
tures of two Pseudomonasspp. (83),
and 2-chloropyridine is embodied
both in the potent enediyne antitu-
mor agent kedarcidin (84) and in
the novel Ecuadoran poison frog
metabolite (Structure 30), which is
secreted by several species of Epipe-
dobotes and which has powerful
analgesic activity (85).
Aromatic compounds. Although
most of nature's chlorinated aro-
matic rings are phenolic, a few ex-
amples of simple chlorinated aro-
matics are known. The Mississippi
salt marsh "needlerush" Uuncus ro-
emerianus) contains 1,2,3,4-tetra-
chlorobenzene (86).A careful study
of the ash from the 1980 eruption of
Mt. St. Helens has revealed the pres-
ence of chloroaromatics (Structures
31 and 32), and, more surprisingly,
three previously unknown isomers
of pentachlorobiphenyls (PCBs)
(Structure 33). The nature of the
PCB isomers is not what would be
expected from industrial PCBs (87).
This landmark observation repre-
sents the first (and only) discovery
of natural PCBs. The authors sur-
mise that rapid, incomplete high-
temperature combustion of chlo-
ride-containing plant material in
the eruption zone led to these chlo-
rinated aromatics, as well as to chlo-
romethane. Plants typically contain
200-10,OOO ppm of chloride ion
(12). Another unusual discovery is
 and another Nostoc sp. blue-green
alga secretes large quantities of two
iBLE 2 chlorinated phenolic furanones,
iogenic sources of simple haloalkanes nostoclides I and 11, into the culture
medium (99). The acorn worm Pty-
mpound Sources chodera bahamensis produces 1 3
1,CI Mar ne a.gae. giant nelp. YOOO ion ng lm 2s halogenated phenols, including 3,4-
ce p ant. c. tivatea mLshrooms wn le cecfar dichloro- and 3,5-dichlorophenol
oenc cedar. everoreen cvoress lmai. (ZOO). The mixed bromochlorodi-
phytoplankton. lorest firei,bush burrhg
volcanoes, tobacco smoke phenyl ether (Structure 40) is pro-
Oceans, marine algae, giant kelp, volcanoes duced by a marine sponge and ac-
Oceans, marine algae, volcanoes counts for 1.3% of the dry weight
Marine algae, white cedar, lemon, orange,
(202). It is interesting to note that
moss, barley, volcanoes, drill wells this compound is a predioxin in-
Marine algae, oceans termediate. The red alga Rhabdonia
Marine algae, oceans, volcanoes, drill wells verticillata produces six bromo1
Volcanoes, barle chloro phloroglucinols (102).
Dioxins and related compounds.
Dioxin, 2,3,7&tetrachlorodiben-
zo-p-dioxin (Structure 411, was
Marine algae, oceans
once generally thought to be the
most toxic man-made chemical
Marine algae, oceans
known (203-1 05). However, exten-
Marine algae
sive evaluations by epidemiologists
Marine algae, oceans of people exposed to dioxin, such as
Marine algae Vietnam veterans (106,207), inhab-
Marine algae, oceans itants of Seveso, Italy [the site of a
3r major dioxin release in 1976 (20811,
I and industrial plant workers (109.
421 110),have revealed that dioxin is
not the doomsday chemical once
iBrlCI believed (210-122).Nevertheless,
iBr12 the extraordinary toxicity of some
,C=CHCI polychlorinated dioxins (PCDDs)
,C=CCI, Oceans, volcanoes and related compounds, such as the
i,CCI, Oceans polychlorinated dibenzofurans (PC-
iFCI, Volcanoes DFs) (e.g., Structure 42), in some an-
=CIS Volcanoes, drill wells imals is reason enough for the con-
tinued study of these compounds,
-IF& especially because it is now recog-
iFCI, nized that PCDDs and PCDFs are, in
,C=CF,
fact, natural products and are ubiq-
uitous in our environment.
1 X=CF,
CCI,FCCIF,
The production of chloromethane
a n d other organochlorine com-
pounds when organic material is
burned, in association with the om-
that an unidentified deep-sea gorgo- (92), have been reported. nipresent chloride ion (see above),
nian, collected at a depth of 350 m, Chlorophenols are used industri- led to the belief, now supported by
exudes haloazulenes (Structure 34) ally on a large scale and have been evidence, that PCDDs could form
(88). classified by EPA as Priority Pollut- during combustion processes ( I 23,
Phenols and phenolic ethers. A ants (93). Surprisingly, several of 214). Laboratory studies have re-
number of chlorinated tyrosine de- these and other chlorophenols are vealed that PCDDs, including di-
rivatives have been isolated from produced naturally. The soil fungus oxin (Structure 421, and PCDFs
marine sponges, seafans, and other Penicillium sp. produces 2,4-di- form in parts-per-billion amounts
gorgonians (89-90). These amino chlorophenol (Structure 36) (94). during the combustion of wood
acids, when incorporated into and grasshoppers secrete 2,5-di- (treated or untreated) (125-218).
structural proteins, may stabilize chlorophenol (Structure 37), which The relatively poor efficiency and
the proteins in the organism by im- is repellent to ants (95). The sex incomplete oxidation when damp
proving the adhesion between pro- pheromone of the female Lone Star vegetation and wood are burned in
tein fibers and sheets (90). The mol- tick (Amblyomma americanurn) the presence of high chloride con-
lusk Buccinum undatum utilizes and several other hard ticks is 2,6- centrations (70-2100 ppm in wood
3-chloro-5-bromotyrosine (Struc- dichlorophenol (Structure 38) (96, pulp) (14) are conditions conducive
ture 35) in its structural proteins 97). Careful studies in the first and to PCDD formation, and two re-
(90). The isolation of 3.4-dichloro- last of these investigations rule out search groups have concluded that
tyrosine, as well as Structure 35, the possibility that these com- forest and brush fires are the major
from Limulus polyphemus @I),and pounds are artifacts. The blue-green source of PCDDs and PCDFs in the
of 3-chlorotyrosine from the cuticle alga Anacystis marina contains environment (125, 229). It is esti-
of locusts (Schistocerca gregaria) chlorophenol (Structure 39) (98), mated that some 130 lb [l lb =

Environ. Sci. Technol., VoI. 28, No. 7, 1994 315 A

0.4536 kg] of PCDDs are produced
in Canadian forest fires annually
( 1 2 9). This is 10 times more than the
amount formed in the 1976 Seveso
plant accident. Because most forest
fires are lightning-caused, and there
are 200,000 forest fires annually
worldwide that burn 27,000 square
miles [l mi = 1.609 km] ( 2 4 ) , it is
logical to assume that PCDDs have
been present in the environment for
many centuries. An 1877 soil sam-
ple was found to contain PCDDs
and PCDFs (220).
Another milestone observation is
the enzymatic conversion of chloro-
phenols into both PCDDs a n d
PCDFs i n the parts-per-million
range by horse-radish peroxidase
enzyme (HRP) (Equation 1) ( 2 2 2 ) .
This extraordinary revelation opens
the door to the possibility that a
source of environmental PCDDs and
PCDFs may be their completely
natural formation from (natural)
chlorophenols by soil and water mi-
crobes.
peroxidase enzymatic activity
(2251, a n d chloroperoxidase,
which occurs in the mold Caldar-
iomyces fumago, has been exten-
sively studied ( 2 2 6 ) . Soil extracts
have been shown to have chlori-
nating ability ( 2 2 2 , 2 2 7 ) , and more
than 80 species of Death Valley
fungi displayed chloroperoxidase
activity ( 1 2 2 ) . Peroxidases are
present in the thyroid gland of
mammals ( 2 2 8 ) .The enzymes chlo-
roperoxidase, HRP, and vanadium
peroxidase are capable of chlorinat-
ing phenols and phenol ethers (ani-
sole) in the presence of chloride
(229, 230). Lactoperoxidase, an en-
zyme present in mammalian milk
( 2 3 2 ) ,is capable of chlorinating or-
ganic substrates (129, 2 3 2 ) .
An electrifying development is
the utilization of the halide-peroxi-
dase-hydrogen peroxide chemical
system by humans and other mam-
mals to generate active halogen
(HOC1, HOBr) in order to destroy
microorganisms. T h u s , human
white blood cells (eosinophils and
neutrophils) contain myeloperoxi-
dase, which, in the presence of
Natural versus anthropogenic
organohalogen compounds
Chloromethane is overwhelm-
ingly biogenic in origin. But what
about the relative quantities of the
other natural organochlorines and
organohalogens vis-&-vis the ap-
proximately 20 million tons per
year of 150 industrial organohalo-
gens currently in use worldwide
(222, 242)? A detailed study of the
acorn worm Ptychodera flava has
revealed that a known population of
these animals (64 million) excrete
in their fecal matter 95 lb of organo-
halogens daily in a 1 km2 habitat in
Okinawa ( 2 4 3 ) . Obviously, many
more studies of a similar nature are
needed in order to estimate the glo-
bal quantities of natural organo-
halogens.
Several researchers have reported
the identification of halogenated
phenolic compounds in ocean wa-
ters and in soil extracts (129, 244,
2 4 5 ) . The major source of most of
these compounds, such as 2,4,6-
trichlorophenol, is biogenic and
from natural halogenation pro-

p -
OH
HRP
H202
CI 17h,2OoC
CI
PCDDs
PCDFs
(38 compounds identified; (214, CIS,Cl6
isomers dominate; ppm range)
Mechanisms of biogenic
chlorination
Marine organisms, terrestrial
plants, fungi, microorganisms, and
mammals all contain haloperoxi-
dase enzymes that can chlorinate,
brominate, and iodinate organic
compounds i n the presence of
chloride, bromide, or iodide ions,
respectively ( 2 2 2 - 2 2 4 ) . Of 33 spe-
cies of Phaeophyceae algae from
the Atlantic Coast, 2 2 displayed
chloride, bromide, or iodide, and cesses such as reactions between
hydrogen peroxide, rapidly forms humic acid and soil microbes (chlo-
active halogen, resulting in the ride and chloroperoxidase). Humic
death of bacteria and fungi by halo- acids are present not only in soil,
genation reactions ( 2 3 2 , 2 3 3 ) . It but also in rivers, lakes, and the
would appear that biohalogenation oceans ( 2 4 6 ) . The yearly net pro-
is an integral component of our im- duction of environmental humic
mune system! acid from the decomposition of or-
ganic material has been estimated at
Metabolism and biodegradation 63 billion tons ( 2 4 6 ) . This can be
Contrary to common perception, added to the estimated existing glo-
organohalogen compounds, both bal 1.0-1.5 trillion tons of soil hu-
mic acids and one trillion tons of
natural and unnatural, are readily
metabolized and biodegraded to ha- ocean humic acid ( 2 4 6 ) .Numerous
lide ion by assorted microorgan- studies have demonstrated the ease
isms. The simple organochlorines with which humic acid model com-
CH,Cl,, CHCl,, CCl,, Cl,C=CC1,, pounds (phenolics)react with chlo-
and others can be degraded to CO, rine to produce chloroform and
(or other simple organics) and chlo- other simple organochlorines via
ride by soil bacteria ( 2 3 4 ) .The soil chlorophenols ( 2 46-2 4 8 ) . As we
bacterium Pseudomonas putida ox- have seen, chloride is ubiquitous in
idizes chloro- and other haloben- soil, plants (200-10,000 ppm) (221,
zenes to the cis-diol ( 2 3 5 ) .This is a rivers (average 8 ppm) ( 2 4 9 ) ,lakes
remarkably general reaction and ( 2 4 9 ) , and, of course, oceans (146,
succeeds even with fluorobenzene. 249). These ingredients, in combi-
The biodegradation of chlorophe- nation with natural chloroperoxi-
nols has been thoroughly studied. dase and other enzymes, provide a
For example, 2,4-dichlorophenol is plausible rationale for the natural
rapidly metabolized in soils ( 2 3 6 ) , formation of chlorinated phenols.
and an exhaustive mechanistic Several studies have demonstrated
study of the degradation of this that the natural production of chlo-
compound to chloride and CO, by rinated phenols and anisoles out-
the white-rot fungus Phanerochaete weighs their anthropogenic sources
chrysosporium has been reported (244, 245).
( 2 37).This versatile and remarkable Although a vast number of halo-
fungus is capable of degrading other genated compounds have been iso-
chlorinated phenols ( 2 3 8 ) , DDT lated from natural sources ( 3 ) ,rela-
( ~ 3 9 pentachlorophenol
), ( 2 4 0 ) ,and tively few marine organisms have
PCBs (142). been examined for their chemical

316 A Environ. Sci. Technol., Vol. 28, No. 7 , 1994

content. For example, whereas
some 12,000 natural products of all
types have been isolated from ter-
restrial plants, only 500 had been
isolated from marine plants (algae)
up to 1987 ( 1 5 0 ) .However, there are
some 500,000 known species of ma-
rine animals, plants. and bacteria
(151). For example, there are 80.000
living species of mollusks (152).
5000 species of sponges (1531, and
4000 species of bryozoans [moss an-
imals) (154). but only six of the lat-
ter have been examined (155). Of
more than 90 known species of
deep-sea gorgonians in the Hawai-
ian Islands, only 20 have been in-
vestigated for their chemical con-
tent ( 1 5 6 ) . a n d . of 1 3 Mycole
sponges living in the Mediterranean
Sea, only one has been investigated
(157). The list goes on.
The enormous diversity of marine
life and, hence, of potential new or-
ganochlorine compounds, is epito-
mized by the Great Barrier Reef.
This 100,000-mi' area consists of
2500 separate small reefs. Around
just one of these, of less than 1 4
square miles, there have been iden-
tified 930 species of fish: 107 corals:
and 154 urchins, cone shells, and
other mollusks (156). Given such
diversity and magnitude of biologi-
cal species, it is indisputable that a
large number of unique organochlo-
rine compounds will be isolated
and identified from ocean life, to
say nothing about the novel chlori-
nated and other halogenated com-
pounds waiting to be discovered in
terrestrial plants, animals, bacteria,
fungi, and perhaps even humans.
Indications are that organohalo-
gen compounds have been with us
for centuries. For example. haloge-
nated fulvic acids have been iso-
lated from groundwater samples
that date hack 1300,4600, and 5200
years (244)! Organohalogen mate-
rial was identified in sediments dat-
ing back to the 13th century (159).
Microfossils in Precambrian rocks,
which are a billion years old, are
identical to the blue-green alga Nos-
toc, and other microfossils are mor-
phologically indistinguishable from
Oscillotoria. two present-day spe-
cies rich in organohalogen com-
pounds (160).
Function of natural
organohalogens
Why does nature create organo-
chlorine compounds? Many marine
and terrestrial organisms use or-
ganochlorine and other organohalo-
gen compounds i n chemical de-
fense-feeding deterrents, irritants,
or pesticides-or in food gathering
(161-164). A recent, careful study
of the sea hare St~vlocheiluslongi-
couda clearly indicates a feeding
deterrent role for its organohalogen
compounds (165). The sea hare
Apl.vsia brnsiliann is distasteful to
fish and rejected by sharks in part
because of its panacene. a bromi-
nated allene ( 1 6 6 ) . Marine algae
store organohalogen compounds in
the vesicular cells for facile secre-
tion to discourage predators (27,
167). and the terrestrial blue-green
alga Fischerello ombiguo secretes
into the medium two chlorinated
phenols that show antibacterial, an-
tifungal, and molluscicidal activity
(166). The marine algae metabolite
telfairine (Structure 5 ) is 100% le-
thal to mosquito larvae at 10 ppm
(1691, and the related chlorinated
monoterpene plocamene B is three
times more effective than the com-
mercial pesticide Lindane against
mosquito larvae (170). An organo-
bromine compound with natural in-
secticidal properties (against the
cotton boll weevil) was recently iso-
lated from the Thai plant Arundo
donax (171). and the coral Tubos-
troea microntha secretes two or-
ganobromine compounds that deter
the destructive crown-of-thorns sea
star from feeding ( 1 72). Recently, it
was found that the German cock-
roach (Blottello germonico) utilizes
two chlorinated steroid glycosides,
blattellastanosides A and B, as ag-
gregation pheromones (173).
One very attractive hypothesis is
that natural organohalogen com-
pounds play an essential role in the
survival of the organism, and the
1
i
1. i.
~
~,
i
;2&
4 1 1 SOC.1973. 60. 347.
. .~ T , ' , ~
Gordon W. (;ribbk! is n professor and
former choir mu^^ 0 1 the llepnrtn~entof
C1tentistl:t~111 l~urtntouthCollege. He re-
ceived his B.S.degree from the Univer-
sity of California-Berkelev and his Ph.D.
from the University of Oregon. After o
year at UCLA os n National Cancer lnsti-
tule Posfdocforal Fello~,,he joined the
faculty of Dartmouth College in 1968.
His research interests include the syn-
thesis and isolation of biologically ac-
tive natural products, heterocyclic
chemistry, and environmental organic
chemistry.
Environ. Sci. Technol.. Vol. 28,No. 7. 1994 317 A
ability of the organism to synthesize
such compounds for chemical de-
f e n s e and food gathering has
evolved over time under the stress
of natural selection (174).
Conclusion
The continued improvements in
isolation, purification, and spectro-
scopic techniques ensure that even
the most structurally intricate orga-
nohalogen natural products will be
identified. Widespread antibiotic,
antitumor, antifungal. insecticidal.
herbicidal, and other potentially
valuable biological activities have
been observed with these natural
chlorinated chemicals. As our un-
derstanding of biohalogenation
progresses, it will be possible to dif-
ferentiate and quantify more accu-
rately the natural and anthropo-
genic sources of halogenated
chemicals.
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