Electron-Donating Phenolic and Electron-Accepting Quinone

Analysis of anoxic pore water and oxic pool water samples collected across an ombrotrophic bog in Sweden demonstrated the presence of both phenolic an...
0 downloads 0 Views 1MB Size
Subscriber access provided by UNIVERSITY OF TOLEDO LIBRARIES

Environmental Processes

Electron-donating Phenolic and Electron-accepting Quinone Moieties in Peat Dissolved Organic Matter: Quantities and Redox Transformations in the Context of Peat Biogeochemistry Nicolas Walpen, Gordon James Getzinger, Martin H. Schroth, and Michael Sander Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b00594 • Publication Date (Web): 28 Mar 2018 Downloaded from http://pubs.acs.org on March 29, 2018

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 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 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.

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 30

Environmental Science & Technology

1

Manuscript

2

Electron-donating phenolic and electron-accepting quinone moieties in peat

3

dissolved organic matter: quantities and redox transformations in the context of

4

peat biogeochemistry

5 6 7

NICOLAS WALPEN, GORDON J. GETZINGER, MARTIN H. SCHROTH, AND MICHAEL SANDER*

8 9

Institute of Biogeochemistry and Pollutant Dynamics,

10

Department of Environmental Systems Science,

11

Swiss Federal Institute of Technology (ETH), 8092 Zurich, Switzerland

12 13 14

Submitted as manuscript to Environmental Science & Technology

15 16 17 18 19 20

*Corresponding author: Michael Sander Email: [email protected] Phone: +41 44 632 83 14

21 22 23 24 25

Number of pages: 29 Number of figures: 4 (total of 1800 word equivalents) Number of tables: 0 Number of words: 5789 Total Number of word equivalents: 7589

1 ACS Paragon Plus Environment

Environmental Science & Technology

26

Page 2 of 30

ABSTRACT

27

Electron-donating phenolic and electron-accepting quinone moieties in peat

28

dissolved organic matter (DOM) are considered to play key roles in processes

29

defining carbon cycling in northern peatlands. This work advances a flow-injection

30

analysis system coupled to chronoamperometric detection to allow for the

31

simultaneous and highly-sensitive determination of these moieties in dilute DOM

32

samples. Analysis of anoxic pore water and oxic pool water samples collected across

33

an ombrotrophic bog in Sweden demonstrated the presence of both phenolic and

34

quinone moieties in peat DOM. The pore water DOM was enriched in phenolic but

35

not quinone moieties compared with commonly used model aquatic and terrestrial

36

DOM isolates. Significantly lower phenol content in DOM from oxic pools than

37

DOM from anoxic pore waters indicated oxidative DOM processing in the pools.

38

Consistently, treatment of peat DOM with laccase, a phenol-oxidase, under oxic

39

conditions resulted in irreversibly removal of phenols and reversible oxidation of

40

hydroquinones to quinones. Electron transfer to peat DOM was fully reversible over

41

an electrochemical reduction and subsequent O2-reoxidation cycle, supporting that

42

quinones in peat DOM serve as regenerable microbial electron acceptors in peatlands.

43

The results advance our understanding of redox processes involving phenolic and

44

quinone DOM moieties and their roles in northern peatland carbon cycling.

2 ACS Paragon Plus Environment

Page 3 of 30

Environmental Science & Technology

45

TOC ART

46 47

3 ACS Paragon Plus Environment

Environmental Science & Technology

48

Page 4 of 30

INTRODUCTION

49

Northern peatlands store an estimated 500 ± 100 Pg of carbon1 in the form of

50

peat organic matter (OM) and therefore represent a significant global carbon pool.

51

OM has accumulated in these systems since the end of the last glaciation due to slow

52

plant material decomposition1 resulting from water-logged, anoxic conditions below

53

the peat surface and low average annual temperatures.2-5 Northern peatlands include

54

ombrotrophic bogs characterized by oligotrophy and low pH, two factors that further

55

contribute to slow OM decomposition. Because of the large amount of carbon stored

56

in northern peatlands, it is critical to understand processes that perturb carbon

57

balances in these systems. This is particularly true for processes that lead to the

58

release of stored carbon as carbon dioxide and methane, with potentially severe

59

implications for global warming,6-8 and as dissolved organic matter (DOM) into

60

receiving watersheds.9,10

61

Two processes that affect carbon cycling in northern peatlands center around

62

electron transfer reactions from electron-donating phenolic and to electron-accepting

63

quinone moieties in peat DOM, respectively. The first process is the oxidation of

64

phenolic peat DOM (hereafter referred to as ‘phenols’ which include mono-

65

hydroxylated aromatics as well as hydroquinones). These phenols are produced by

66

Sphagnum mosses11,12 —the dominant peat-forming plant genus in northern

67

peatlands2,4— and are released, either actively or during moss decomposition, to peat

68

pore waters where they purportedly inhibit extracellular hydrolases and thereby slow

69

OM decomposition.13-16 In anoxic pore waters, low activities of phenol-oxidizing

70

(per)oxidases, which require oxygen or peroxide as co-substrates, render phenols

71

stable.17 The so-called ‘enzymic latch’ hypothesis posits that increased (per)oxidase

72

activity caused by more frequent peat oxygenation events through water table draw-

4 ACS Paragon Plus Environment

Page 5 of 30

Environmental Science & Technology

73

down in a warming climate14 could remove phenols and thus their inhibitory pressure

74

on hydrolase activity, thereby triggering OM decomposition and thus significant

75

releases of carbon from northern peatlands.14,18-20

76

The second process is the reduction of quinone to hydroquinone moieties

77

(hereafter referred to as ‘quinones’) in peat DOM: quinones may be used as electron

78

acceptors for anaerobic microbial respiration,21-25 including anaerobic methane

79

oxidation.26-29 As a result, quinone reduction is considered to significantly suppress

80

methane emissions from northern peatlands.5,30-34 This suppression may be

81

sustainable over longer time periods if the formed hydroquinones are oxidized back to

82

the electron-accepting quinones through electron transfer to oxygen at anoxic-oxic

83

interfaces in the peat35 or to peat particulate OM, akin to DOM electron shuttling in

84

dissimilatory iron oxide reduction.22,36,37 While reversible electron transfer to peat

85

DOM would thus have large implications for methane emissions from northern

86

peatlands, this process has not yet been experimentally demonstrated.

87

Despite the key role of phenols and quinones in the above processes, little

88

information was heretofore available on the quantities and redox transformations of

89

these moieties in peat DOM. Obtaining this information has, to a large part, been

90

impaired by the lack of a sufficiently sensitive analytical technique to quantify these

91

moieties

92

chronoamperometric analyses in electrochemical cells, the heretofore most sensitive

93

approach to quantify phenols24,38 and quinones23,24, require samples with DOM

94

concentrations above those commonly found in natural systems. To supersede these

95

analytical challenges, we recently introduced a flow-injection analysis (FIA) system

96

to quantify phenols in DOM samples containing only a few milligrams carbon per

97

liter.39 We used the FIA system to quantify phenols in peat DOM in a small set of

in

samples

with

low

DOM

concentrations.

Even

mediated

5 ACS Paragon Plus Environment

Environmental Science & Technology

Page 6 of 30

98

water samples collected in three Swedish ombrotrophic bogs and to monitor peat

99

DOM enzymatic oxidation.39 However, the inability of the original FIA system to

100

quantify the number of electrons transferrable to DOM precluded a comprehensive

101

assessment of peat DOM redox properties and transformations, including the

102

quantification of electron accepting quinones and the analysis of electron transfer

103

reversibility during peat DOM oxidation and reduction.

104

The objectives of this work were (i) to extend the previously-introduced FIA

105

system for additionally quantifying the electron-accepting moieties in dilute DOM

106

samples and to validate and assess the performance of the extended system, (ii) to

107

systematically characterize variations in the geochemical and redox properties of peat

108

DOM samples collected across a peatland and to compare these redox properties with

109

those of well-characterized model DOM isolates, and (iii) to assess the reversibility of

110

electron transfer from and to phenols and quinones in peat DOM during enzymatic

111

oxidation and over an electrochemical reduction and O2-reoxidation cycle,

112

respectively. For objectives (ii) and (iii), we collected and analyzed 29 pore and 30

113

pool water DOM samples from an ombrotrophic bog in central Sweden. This work

114

provides heretofore missing information on the quantities and the transformations of

115

phenols and quinones in peat DOM and thereby advances a more holistic

116

understanding of redox processes involving peat DOM that impact carbon cycling in

117

northern peatlands.

118

MATERIALS AND METHODS

119

Chemicals and enzymes. Potassium chloride, potassium phosphate dibasic

120

trihydrate, potassium phosphate monobasic, sodium acetate trihydrate, acetic acid,

121

(+)-sodium

L-ascorbate,

disodium

9,10-anthraquinone-2,6-disulfonate,

and

6 ACS Paragon Plus Environment

Page 7 of 30

Environmental Science & Technology

122

diammonium

2,2'-azino-bis(3-ethyl-6-benzothiazolinesulfonate)

123

obtained

124

(Zwitterionic viologen, ZiV) was synthesized and purified as described elsewhere.40

125

Laccase from Trametes versicolor was obtained from Fluka (activity: 22.4 U·mg-1;

126

product number 53793) and used as received. Aqueous laccase stock solutions (5

127

U·mL-1) were freshly prepared for each experiment.

from

Sigma-Aldrich.

(ABTS)

were

N,N'-bis(3-sulfonatopropyl)-4,4'-bipyridinium

128

Solutions. All solutions were prepared in ultrapure water (resistivity >18.2

129

MΩ·cm) obtained from a Barnstead Nanopure Diamond system. FIA system carrier

130

solutions were buffered with 0.1 M phosphate or 0.1 M acetate for analyses at pH 7

131

and 5, respectively. The FIA reagent solutions contained the chemical reductant ZiV•-

132

(i.e., reduced ZiV in 1 mM phosphate, pH 7) and the oxidant ABTS•+ (i.e., oxidized

133

ABTS in 1mM acetate, pH 3.9), respectively, and 0.1 M KCl as electrolyte. All

134

solutions were N2-sparged for two hours before transferring into the anoxic glove box

135

(N2 atmosphere,