ReviewPattern and sources of naturally produced organohalogens in the marine environment: biogenic formation of organohalogens
Introduction
Halogenated compounds found in the environment can be classified as being:
- •
biogenic (e.g. CH3Cl)
- •
natural/geogenic (e.g. specific dioxins in clay)
- •
having anthropogenic non-halogenated precursors (e.g. halogenated phenols formed from phenol)
- •
having anthropogenic halogenated precursors (e.g. chlorophenols formed from chlorobenzenes, pentachlorophenyl methyl ether formed from pentachlorophenol), or
- •
anthropogenic (e.g. freons, CH3CCl3, PCBs, POPs).
Since the identification of 6,6′-dibromoindigotin (Tyrian Purple) in marine snails in 1909, a variety of biogenic carbon–halogen compounds has been detected in algae, fungi, plants and biota. The wide spectrum of natural halogenated compounds has been summarized in the past by several authors (Doonan , 1973; Fenical, 1982; Faulkner, 1984; Neidleman and Geigert, 1986; Grimvall and de Leer, 1995; Gribble, 1996, Gribble, 1998, Gribble, 1999).
Recently the group of persistent organic pollutants, the so-called POPs, which are mostly semivolatile chlorinated compounds, have gained wide political visibility thanks to actions of the UN. Ballschmiter summarized the possible spectrum of compounds that have to be discussed in this respect (Ballschmiter et al., 2001).
Polyhalogenated bi-pyrrols identified in the marine environment can be described as natural POPs, persistent organic pollutants. These halogenated 2,2′-bipyrroles, e.g. C10H6N2Br4Cl2, a 1,1′-dimethyl-tetrabromodichloro-2,2′-bipyrrole accumulate e.g. in fish, birds and marine mammals like the PCBs. (Gribble et al., 1999; Tittlemier et al., 1999, Tittlemier et al., 2002a, Tittlemier et al., 2002b). A C9H3N2Cl7 compound (Q1/U3) has also been identified as a bioaccumulating natural product (Weber and Goerke, 1996; Vetter, 1999; Vetter et al., 1999, Vetter et al., 2000). The compound C9H3N2Cl7 (Q1/U3) is a heptachloro-1′-methyl-1,2′-bipyrrole (Wu et al., 2002). A similar global spreading through the marine biosphere as it is observed for the PCBs has not been found yet for this natural heptachlorinated 1,2′-bipyrrol (Hackenberg et al., 2001). Vetter also reported a mixed halogenated trichlorodibromo-compound in fish and seal (Vetter et al., 2001). It was tentatively assigned to a monoterpene structure.
The occurrence of natural organohalogens resembling the PCB structure, specifically a broad spectrum of volatile and bioaccumulative organohalogens, has stimulated a renewed interest in the chemistry of formation of natural organohalogen compounds under environmentally conditions. It has been known for long that fungi, for example, produce chlorophenols (Turner, 1971). The higher chlorinated compounds of this group are considered as classical anthropogenic compounds found in the environment. Even the natural formation of dioxins of the 2,3,7.8-type has been reported (Svenson et al., 1989; Hoekstra et al., 1999; Ferrario et al., 2000).
Section snippets
Biogenic fluorinated compounds
Biogenic formation of fluoro-organic compounds is mainly of theoretical relevance, though the rare organofluorine compounds are more widely spread in nature than originally presumed. F-metabolites have been discovered in bacteria, fungi (Streptomyces sp.) and higher plants but not yet in algae (Neidleman and Geigert, 1986; O’Hagan and Harper, 1999; O’Hagan et al., 1999). The toxic monofluoroacetate is found in numerous higher plants at the trace level. Ceylon tea may contain 50–160 ng/g
Volatile organohalogens in the marine environment
For natural organohalogen compounds found in the marine environment Br mostly dominates over Cl, while for natural organohalogens found in the terrestrial environment Cl dominates over Br. The volatile organohalogens like the methane derivatives CH3Cl, CH3Br, CH3I, CH2Cl2, CH2Br2, CH2I2, CH2ClBr, CH2ClI, CHCl3, CHBr3, CHBrCl2, CHBr2Cl, several halogenated ethanes and acetones, and even halogenated methyl-phenyl ethers (anisoles, XzC6H5−z–(OCH3), (X=Br, Cl) can be found worldwide in the marine
Methylation reaction
CH3Cl is by far the most abundant volatile, naturally formed organohalogen. The global atmospheric mixing ratio requires an annual production of 3.5–5 million tons per year of chloromethane (Khalil et al., 1999; Khalil and Rasmussen, 1999a, Khalil and Rasmussen, 1999b; Harper, 2000). The global atmospheric mixing ratio of methyl bromide is substantially lower (Khalil et al., 1993) (Table 2).
The formation of CH3Cl, CH3Br and CH3I is mainly through biomethylation of the respective Cl−, Br− and I−
In vitro incubations with chloroperoxidase (CPO)
To evaluate the possible formation of volatile halogenated C1/C2-hydrocarbons several in vitro incubations with chloroperoxidase (CPO) and horseradish peroxidase (HRP) were carried out with substrate molecules that are common in biochemistry and which possess a carbonyl-activated site (Walter and Ballschmiter, 1991a, Walter and Ballschmiter, 1991b).
The pattern of compounds detected by high resolution capillary gas chromatography and ECD detection is surprisingly high and variable that is formed
Water chlorination chemistry
The similarity of the chemistry discussed above with the basic chemistry of the products formed in water chlorination should be pointed out. In water chlorination as well as in the reaction pathways involving the haloperoxidases, the active species is thought to be HOX (X=Cl, Br, I).
Haloperoxidase reaction: formation of Cl+Water chlorination: formation of Cl+The
Marine areas of high primary production release halomethanes in the Atlantic and the Indian Ocean
Among the volatile halocarbons in the atmosphere the methylhalides CH3Cl, CH3Br and CH3J are known to be mainly of natural origin (Khalil et al., 1993; Khalil and Rasmussen, 1999a, Khalil and Rasmussen, 1999b). The current knowledge of identity and source strength including terrestrian sources explaining the atmospheric concentration of chloromethane has recently been reviewed by Harper (2000).
There has been a long-standing discussion whether CHCl3 besides its anthropogenic sources, which are
Pattern of global occurrence of halogenated phenyl methyl ether (HMPEs; halogenated anisols) in the marine atmosphere
Chlorophenols are normally considered as anthropogenic compounds. Chlorophenols however have been detected in fungi and soil (Hoekstra et al., 1999). The biosynthesis of chloro-metabolites by fungi has been extensively reviewed by Turner (1971).
Bromophenols are quite often found as chemical repellants in marine biota. Methylation of phenols leads to the quite volatile anisols that can be detected in the marine atmosphere on a global scale (Table 4) (Walter and Ballschmiter, 1991a, Walter and
Polychlorinated long chain (C22/C24) hydrocarbons
Unusual hexachlorinated aliphatic C22 and C24 compounds (sulfolipids) are found in phytoflagellatae. They contain two CH–OSO3– groups, and one CH2–CCl2–CH2 moiety, one CH2–CHCl–CHCl–CH2 moiety, and one CH2–CHCl–CH2–CHCl–CH2 moiety (Mercer and Davies, 1979). No biochemical pathway of formation of the different (C–Cl) moieties of these polychlorinated C22–C24 sulfolipids can be given yet.
Formation of halo n-(C1–C3) alkanes by abiotic Fe3+ oxidation of organic matter––a non-biogenic natural process
Phenolic moeities of natural organic matter containing alkoxy groups can be oxidized without microbial mediation in the presence of Fe3+ that is reduced to Fe2+. During this process halides are C1–C3 alkylated. Methoxy-, ethoxy-, and propoxy groups of phenolic structures apparently lead to the corresponding methyl-, ethyl-, and n-propyl halides (Cl, Br, I) (Keppler et al., 2000). Details of the reaction mechanism are still open.
Classical anthropogenics as naturally produced organohalogens?
Tetrachloromethane, as well as tri- and tetrachloroethene, and hexachloroethane are normally considered as classical man-made organic atmospheric pollutants (e.g. Singh et al., 1976; Kirschmer et al., 1983; Fogelqvist, 1985; Class and Ballschmiter, 1986, Class and Ballschmiter, 1987a, Class and Ballschmiter, 1987b; Wiedmann et al., 1994; Weifl, 1996; Kleiman and Prinn, 2000). The possible natural formation of tetrahalomethanes may involve a radical mechanism (Gribble, 1996; Urhahn and
Conclusions
The spectrum of natural volatile organohalogens seems rather well established in its qualitative aspects, though single new compounds may be found in the future. It is surprising that the detailed reaction pathways of the formation of quite simple volatile organohalogens often are not known. On the other side, the chemistry of the group of haloperoxidases as seen in incubation experiments reveals that a wide spectrum of unknown compounds is formed in side reactions in pathways not yet
References (109)
- et al.
Vanadium haloperoxidases from brown algae of the Laminariaceae family
Phytochemistry
(2001) - et al.
A Chloroperoxidase-like catalyst in soil: detection and characterisation of some properties
Soil Biology Biochemistry
(1993) - et al.
Enzymatic chlorination using bacterial nonheme haloperoxidases
Enzyme and Microbial Technology
(1994) Mechanistic considerations of the vanadium haloperoxidases
Coordination Chemistry Reviews
(1999)- et al.
Distribution of chlorinated C1/C2-hydrocarbons in air over the northern and southern Atlantic Ocean
Chemosphere
(1986) - et al.
Bromo- and bromochloromethanes in air over the Atlantic Ocean
Chemosphere
(1986) - et al.
C1- and C2-halocarbons in soil–air of forests
Atmospheric Environment
(1989) Haloperoxidases––Useful catalysts for halogenation and oxidation reactions
Catalysis Today
(1994)- et al.
Occurrence and formation of chloroform at Danish forest sites
Atmospheric Environment
(2000) - et al.
Formation of chloroform in spruce forest soil––results from laboratory incubation studies
Chemosphere
(2000)
Chloroform-concentration gradients in soil, air and atmospheric air, and emissions fluxes from soil
Atmospheric Environment
Atmospheric methyl chloride
Atmospheric Environment
Atmospheric chloroform
Atmospheric Environment
Die Belastung der unteren Troposphäre mit C1–C6 Organohalogenen
Chemosphere
Haloperoxidases and their role in biotransformation reactions
Current Opinion in Chemical Biology
Distribution of chlorosulpholipids in algae
Phytochemistry
Fluorine-containing natural products
Journal of Fluorine Chemistry
Dihaloacetonitriles in Dutch drinking waters
Water Research
Haloperoxidase activity of manganese peroxidase from Phanerochaete chrysosporium
Archives of Biochemistry and Biophysics
Structure elucidation of four possible biogenic organohalogens using isotope exchange mass spectrometry
Chemosphere
Examination of the bioaccumulation of halogenated dimethyl bipyrroles in an Arctic marine food web using stable nitrogen isotope analysis
Environmental Pollution
Chemistry of the biosynthesis of halogenated methanes: C1-organohalogens as pre-industrial chemical stressors in the environment
Chemosphere
Bacterial haloperoxidases and their role in secondary metabolism
Biotechnology Advances
The determination of traces of fluoro-acetic acid by extractive alkylation and pentafluorobenzylation and capillary-gas chromatography-mass spectrometry
Analytica Chimica Acta
Determination of Q1, an unknown organochlorine contaminant, in human milk, Antarctic air, and further environmental samples
Environmental Pollution
Formation and distribution of halogenated volatile organics in sea water
The natural formation of trichloroethylene and perchloroethylene in sea water
Alkyl nitrates, nonmethane hydrocarbons, and halocarbons gases over the equatorial Pacific Ocean during SAGA-3
Journal of Geophysical Research
Transport and fate of organic compounds in the global environment
Angewandte Chemie Int Ed Engl
Man-made chemicals found in remote areas of the world: The experimental definition for POPs
ESPR––Environ Science & Pollution Research
Ozone destruction and photochemical reactions at polar sunrise in the lower Antarctic atmosphere
Nature
Dihaloacetonitriles in chlorinated natural waters
Volatile halogen compounds in the alga Asparagopsis Taxiformis
Journal Food Chemistry
Marine haloperoxidases
Chemical Reviews
Evidence of natural marine sources for chloroform in regions of high primary production
Fresenius Zeitschrift für Analytische Chemie
Global baseline pollution studies X. Atmospheric halocarbons: global budget estimations for tetrachloroethene, 1,2-dichloroethane, 1,1,1,2-tetrachloroethane, hexachloroethane and hexachlorobutadiene. Estimation of the hydroxyl radical concentrations in the troposphere of the northern and southern hemisphere
Fresenius Zeitschrift für Analytische Chemie
Sources and distribution of bromo- and bromochloromethanes in marine air and surface water of the Atlantic Ocean
Journal of Atmospheric Chemistry
A Functional model for vanadium, haloperoxidase
Journal of the American Chemical Society
Functional models for vanadium haloperoxidase––reacitvity and mechanism of halide oxidation
Journal of the American Chemical Society
Halomethane: bisulfide/halide ion methyltransferase, an unusual corrinoid enzyme of environmental significance isolated from an aerobic methylotroph using chloromethane as the sole carbon source
Applied and Environmental Microbiology
The biochemistry of carbon-halogen compounds
Marine natural products: Metabolites of marine algae
Natural Products Reports
Natural products chemistry in the marine environment
Science
2,3,7,8-dibenzo-p-dioxins in mined clay products from the United States: Evidence for possible natural origin
Environmental Science & Technology
Carbon tetrachloride, tetrachloroethylene, 1,1,1-trichloro-ethane and bromoform in Arctic seawater
Journal of Geophysical Research
Halogenation and oxidation reactions with haloperoxidases
Biocatalysis
Bromochloro methoxybenzenes in the marine troposphere of the Atlantic Ocean: A group of organohalogens with mixed biogenic and anthropogenic origin
Environmental Science & Technology
Determination of biogenic halogenated methyl-phenyl-ethers (halogenated anisols) in the picogram m−3 range in air
Fresenius Journal of Analytical Chemistry
Analysis of halogenated methoxybenzenes and hexachlorobenzene (HCB) in marine air in the picogram/m3 range
Chromatographia
Naturally Occurring Organohalogen Compounds––A Comprehensive Survey
Cited by (102)
Hidden dangers: High levels of organic pollutants in hadal trenches
2024, Water ResearchMarine volatile organic compounds and their impacts on marine aerosol—A review
2021, Science of the Total EnvironmentCharacterizing changes of dissolved organic matter composition with the use of distinct feeds in recirculating aquaculture systems via high-resolution mass spectrometry
2020, Science of the Total EnvironmentCitation Excerpt :The presence of the CHNOS group of chemicals can also indicate anthropogenic origins (Kamjunke et al., 2017) and incorporation of sulphur in the CHNO group during the reaction with hydrogen sulphide (H2S) under anaerobic conditions (Vairavamurthy and Mopper, 1987; Perlinger et al., 2002; Heitmann and Blodau, 2006; Gonsior et al., 2011). Chlorinated and brominated chemicals can be naturally occurring in nature, but they can also be released by anthropogenic activity as important environmental contaminants (e.g., chlorinated and brominated flame retardants) (Gribble, 1994, 2000; Ballschmiter, 2003). The ingredients and additives of fish feed, and their inappropriate handling and storage can be a potential source of those contaminants in the system (Carro et al., 2005; Fink-Gremmels, 2012).