Subscriber access provided by GAZI UNIV
Article
Ozone-Activated Halogenation of Mono- and Dimethylbipyrrole in Seawater Abdhesh Kumar, Miles Borgen, Lihini I. Aluwihare, and William Fenical Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b03601 • Publication Date (Web): 06 Dec 2016 Downloaded from http://pubs.acs.org on December 7, 2016
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 20
1
Environmental Science & Technology
Environmental Science and Technology
2 3
Ozone-Activated Halogenation of Mono- and Dimethylbipyrrole in Seawater
4 5
Abdhesh Kumar†,‡, Miles Borgen†§, Lihini I. Aluwihare†§, William Fenical†,‡
*
6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29
†
Scripps Center for Oceans and Human Health, ‡Center for Marine Biotechnology and Biomedicine, §Geoscience Research Division, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California 92093, United States ABSTRACT: Polyhalogenated N-methylbipyrroles of two different structure classes have been detected worldwide in over 100 environmental samples including seawater, bird eggs, fish, dolphin blubber, and in the breast milk of humans that consume seafood. These molecules are concentrated in the fatty tissues in comparable abundance to some of the most important anthropogenic contaminants, such as the halogenated flame-retardants and pesticides. Although the origin of these compounds is still unknown, we present evidence that the production of these materials can involve the direct ozone activated seawater halogenation of N-methylbipyrrole precursors. This observation shows that environmental polyhalogenated bipyrroles can be produced via an abiotic process, and implies that the ozone activated halogenation of a variety of natural and anthropogenic seawater organics may be a significant process occurring in surface ocean waters.
30 31
INTRODUCTION
32
More than 5000 naturally-occurring organohalogen compounds are currently known.1,2 These
33
compounds comprise a large number of structure types including halogenated terpenoids,
34
alkaloids, polyketides, peptides, and others. Halogenation is a known biochemical process in
35
some terrestrial organisms, but it is particularly pronounced in marine plants, animals and
36
bacteria, by virtue of their access to the halogens in seawater as building blocks. However, very
37
few, if any of the biosynthetically-produced organohalogens are found to accumulate in marine
38
life, presumably due to their naturally-evolved biodegradation pathways. Among the molecules
ACS Paragon Plus Environment
1
Environmental Science & Technology
Page 2 of 20
39
that are being accumulated in marine food webs world-wide are a large diversity of conspicuous
40
polyhalogenated N-methylbipyrroles, containing randomly mixed bromine and chlorine
41
substituents.3-16 These compounds have received focused attention because they have been found
42
in over 100 environmental samples, including air samples,4 fish11 and sharks,13 dolphin12 and
43
dugong blubber7 and, remarkably, human breast milk4 where they are among the most abundant,
44
non-PCB and non-DDT contaminants that bio-accumulate in fatty tissues.
45
absence in freshwater sources, except one report of their occurrence in Lake Baikal seals, has
46
been taken as strong evidence of a marine origin.6
17,18
Their general
47 48
Polyhalogenated N-methylbipyrroles are of two types, polyhalo-1,1'-dimethyl-2,2'-bipyrroles
49
(DMBPs) and polyhalo- 1'-methyl-1,2'-bipyrroles (MBPs), which are related structures in which
50
two pyrrole rings are linked by either a carbon-carbon (C1-C1) bond or a carbon-nitrogen (C1-N)
51
bond (Figure 1). Both classes of polyhalobipyrroles are found in Nature with bromine and
52
chlorine in various ratios and at various substitution sites on the bipyrrole skeletons.
53
54 55
Figure 1. Chemical compositions of the major polyhalogenated-N-methylbipyrroles observed
56
world-wide that accumulate in marine fatty tissues and human breast milk.
57 58
Subsequent to the first observation of these compounds, natural abundance radiocarbon
59
measurements by Reddy and co-workers have provided significant support for a natural rather
60
than anthropogenic origin of the carbon skeletons in the polyhalobipyrroles.19 Further, the
61
presence of these contaminants has been observed in archived whale oil produced prior to the
62
industrial era.20 Radiocarbon measurements, however, can only identify a biosynthetic origin of
63
carbon, not how and when halogenation occurs. One unique feature of these two classes of
64
bipyrroles is their random halogenation patterns ranging from 1 to 7 halogen isomers at various
65
positions on the bipyrrole rings.14,17,18 Another significant feature is that these compounds are
ACS Paragon Plus Environment
2
Page 3 of 20
Environmental Science & Technology
66
always N-methylated. To date, no industrial materials even closely related to these bipyrroles can
67
be identified. The consistent presence of chlorine and bromine, and the completely random
68
regiochemistry of halogen substitution, is inconsistent with known biosynthetic halogenation
69
processes which largely target bromination. These processes involve a variety of brominating
70
enzymes that function in a regio- and stereo-chemically specific manner.1,2 Bacteria of the
71
common genus Pseudoalteromonas, for example, are known to brominate, but to not chlorinate
72
pyrroles in natural biosynthetic processes.21-23 Numerous other halogenation products such as the
73
halomethanes CH3I, CH3Br, CH2I2, CH2ICl are known to occur at ppb concentrations in seawater
74
by photochemical halogenation of unknown dissolved organic matter.24-29 Other halogenation
75
reactions, involve the production of halomethanes by seaweeds, albeit also at ppm and ppb
76
levels.25 These observations of very low levels of photochemical halogenation reaction products
77
do not explain the world-wide bioaccumulation of the polyhalo-N-methylbipyrroles. That these
78
bipyrrole contaminants are produced in significant amounts, and bio-concentrated in such a vast
79
diversity of marine life, suggests a prolific and potentially dynamic source in ocean systems.
80 81
The exchange of gases across the air-sea interface provides a primary relationship between the
82
chemistry of the ocean and atmosphere. Many gases (CO, CH4, N2O, H2, O3, methyl halides etc,)
83
and numerous shorter-lived species (
