Relationship of Biodiversity with Heavy Metal Tolerance and Sorption

Nov 27, 2017 - First, the relationship of the maximum sorption capacity, qmax, to the microbial kingdom was investigated with qmax values for various ...
0 downloads 0 Views 1MB Size
Subscriber access provided by Queen Mary, University of London

Article

Relationship of biodiversity with heavy metal tolerance and sorption capacity: A meta-analysis approach Isis E Mejias Carpio, Ali Ansari, and Debora F. Rodrigues Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b04131 • Publication Date (Web): 27 Nov 2017 Downloaded from http://pubs.acs.org on November 29, 2017

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 36

Environmental Science & Technology

1

Relationship of biodiversity with heavy metal

2

tolerance and sorption capacity: A meta-analysis

3

approach

4

Running title: Biodiversity and heavy metal Meta-analyses

5

Isis E. Mejias Carpio a, Ali Ansari a, and Debora F. Rodrigues a,*

6

7

a

Department of Civil and Environmental Engineering. University of Houston, Houston, TX-

8

77004, USA

9

E-mail: [email protected]

10 11

*Corresponding Author: E-mail: [email protected]; Tel: 713-743-1495; Fax: 713-743-4260

12 13

TOC/Abstract Art

14

1 ACS Paragon Plus Environment

Environmental Science & Technology

15

Abstract

16 17

Microbial remediation of metals can alleviate the concerns of metal pollution in the

18

environment. The microbial remediation, however, can be a complex process since microbial

19

metal resistance and biodiversity can play a direct role in the bioremediation process. This study

20

aims to understand the relationships among microbial metal resistance, biodiversity, and metal

21

sorption capacity. Meta-analyses based on 735 literature data points of Minimum Inhibitory

22

Concentrations (MIC) of plantae, bacteria, and fungi exposed to As, Cd, Cr Cu, Ni, Pb, and Zn ─

23

showed that metal resistance depends on the microbial Kingdom and the type of heavy metal,

24

and that consortia are significantly more resistant to heavy metals than pure cultures. A similar

25

meta-analysis comparing 517 MIC values from different bacterial genera (Bacillus, Cupriavidus,

26

Klebsiella, Ochrobactrum, Paenibacillus, Pseudomonas, and Ralstonia) confirmed that metal

27

tolerance depends on the type of genus. Another meta-analysis with 195 studies showed that the

28

maximum sorption capacity is influenced by microbial Kingdoms, the type of Biosorbent

29

(whether consortia or pure cultures), and the type of metal. This study also suggests that

30

bioremediation using microbial consortia is a valid option to reduce environmental metal

31

contaminations.

32

33

Keywords: biosorption, heavy metals, microbial remediation, diversity, consortia

34

35

2 ACS Paragon Plus Environment

Page 2 of 36

Page 3 of 36

Environmental Science & Technology

36

37

1. Introduction

38

In the past decade, multiple studies indicated that microorganisms can serve as potential

39

alternatives for the sustainable remediation of heavy metals in the environment.1,

2

40

investigations showed that microorganisms belonging to different Kingdoms, i.e. Fungi, Plantae,

41

Eubacteria, are very promising for metal remediation.3 It is still unclear, however, whether the

42

microorganisms from these Kingdoms have similar metal tolerance and sorption capacities.

These

43

Most of the metal sorption studies in the literature use pure cultures, and only recently,

44

researchers have been focusing on microbial communities.4, 5 The value of investigating pure

45

cultures for heavy metal remediation is the discovery of the mechanisms of metal resistance and

46

sorption capacity. Yet, pure culture studies are not practical for large-scale processes or realistic

47

for in situ bioremediation, due to the difficulty in maintaining pure cultures and guaranteeing

48

their optimum metal sorption capacity under different environmental conditions. Alternatively,

49

microbial communities could be a more realistic approach for in situ remediation.

50

The investigation of complex microbial communities for the sorption of heavy metals from

51

the environment is promising, yet an unclear solution. Diverse microbial communities exist in

52

the environment and may hold different sorption capacities or unknown mechanisms of metal

53

resistance. But to date, very few studies have focused on understanding how microbial

54

community diversity affects metal sorption.1, 6 In this context, we highlight the value of studying

55

complex microbial communities to understand how biodiversity affects metal sorption processes

56

in large-scale applications.

57

In addition to research in biodiversity, studies in microbial metal tolerance up to date do not

58

explain its effect on heavy metal sorption processes. The metal Minimum Inhibitory 3 ACS Paragon Plus Environment

Environmental Science & Technology

59

Concentration (MIC) of microbial cells is typically used as a first approach to determine the

60

microbial metal resistance. MIC is commonly defined as the lowest metal concentration

61

inhibiting microbial growth.7 Numerous studies have examined the heavy metal tolerance

62

through the MIC of microorganisms isolated from different habitats, and grown under different

63

conditions. But, to date, that large amount of data is still scattered, with no connection between

64

metal resistance and microbial Kingdoms that could serve for a more effective bioremediation

65

process.

66

In this study, we collected 930 values from other literature studies that comprise common

67

cells used for metal sorption and metal tolerance, with aims to: i) correlate microbial metal

68

tolerance, in terms of MIC, the type of metal, the microbial Kingdom, and the bacterial genus ;

69

ii) determine if the growth medium has an influence in the MIC; iii) link microbial metal

70

sorption capacity with the types of metal and the microbial Kingdom; iv) associate the type of

71

metal and the microbial Kingdom with the maximum sorption capacity (qmax); and v) determine

72

if biodiversity has a significant effect on qmax by considering values of consortia and pure

73

cultures. This approach will allow us to gain a better understanding of the role of microbial

74

diversity, metal resistance, and metal sorption in bioremediation processes.

75

2. Materials and Methods

76

Parameters investigated

77

The meta-analyses presented in this study were performed with data collected from the literature.

78

Table 1 summarizes the categorical and dependent parameters applied. The subsequent sections

79

describe the analyses performed with these parameters.

80 81

4 ACS Paragon Plus Environment

Page 4 of 36

Page 5 of 36

Environmental Science & Technology

82 83

Table 1- Number of literature results utilized for each analysis

Dependent Parameters Categorical Parameter

84

Metal Tolerance, MIC

qmax

Microbial Kingdom (Eubacteria, Fungi, Plantae)

735

195

Types of Metal (As, Cd, Cr, Cu, Ni, Pb, Zn) Bacterial Genus (Bacillus, Cupriavidus, Klebsiella, Ochrobactrum, Paenibacillus, Pseudomonas, Ralstonia) Growth Medium (Minimum and Rich)

735

155

517

N/A

735

N/A

Biosorbent Type (Pure Cultures and Consortia)

735

155

N/A: data not available

85

Analyses of Microbial Metal Tolerance relationships to Kingdoms, Bacterial Genus, Types of

86

Metals, and Biosorbent type

87

In this analysis, we collected 735 MIC results from the literature, as presented in Table 1.

88

These MIC values belong to microorganisms from different Kingdoms under aerobic growth

89

conditions. The data collected were analyzed using the ANOVA statistical analysis with Rstudio

90

(see supporting information). In all analyses in this manuscript, the prokaryotic Kingdom of

91

bacteria was treated as separate from Archaea, as stated by Woese and Fox.8

92

The first analysis involved sorting the 735 MIC values into seven heavy metal groups (As,

93

Cd, Cr, Cu, Ni, Pb, and Zn). The ‘type of metal’ was used as a categorical parameter and the

94

MIC values included prokaryotes, eukaryotes, and consortia with both eukaryotic and

95

prokaryotic microorganisms. A natural logarithm transformation of MIC values was done to

96

obtain a normal distribution of the data. The ANOVA statistical analysis was done to determine

97

if there was a statistically significant difference between the MIC values of all metal groups. In

5 ACS Paragon Plus Environment

Environmental Science & Technology

98

addition, the post hoc Tukey’s test was done to find out which metals had the highest and lowest

99

values (see supporting information).

100

In the second analysis, the ‘MIC’ value was used as a dependent parameter and the

101

‘Kingdom’ (Eubacteria, Fungi, and Plantae) as a categorical parameter. Within those values, the

102

analysis included pure cultures as well as consortia with either prokaryotes or eukaryotes, and

103

consortia with both eukaryotic and prokaryotic microorganisms. The data included MIC values

104

of the most common metals used in biosorption studies: As, Cd, Cr, Cu, Ni, Pb, and Zn. Most of

105

the MIC studies used were short-term studies (maximum of 2 to 4 days of incubation). Some of

106

the studies included tolerance assays done in one week and two were done in two weeks to a

107

month. A natural logarithm transformation of MIC values was done to obtain a normal

108

distribution of the data, presented in the supporting information. ANOVA statistical analysis was

109

done to determine if there was a statistical difference among the three Kingdoms. In addition, the

110

post hoc Tukey’s test was done to find out which group had the highest and lowest values (see

111

supporting information).

112

The third analysis involved evaluating 517 MIC values of pure cultures of different bacterial

113

genera. This analysis aimed to determine whether specific genera could have different metal

114

resistance. The most common genera of bacterium found to resist high concentrations of heavy

115

metals are Acidithiobacillus sp., Desulfovibrio sp., E. coli sp., Cupriavidus sp., Ochrobactrum

116

sp., Streptomyces sp., Micrococcus sp., Acinetobacter sp., and Pseudomonas sp.. However,

117

because not enough data was available for all these genera, we utilized the most commonly

118

studied microbes: Bacillus sp., Cupriavidus sp., Klebsiella sp., Ochrobactrum sp., Paenibacillus

119

sp., Pseudomonas sp., and Ralstonia sp, as categorical parameters. A natural logarithm

120

transformation of MIC values was done to obtain a normal distribution of the data. The ANOVA 6 ACS Paragon Plus Environment

Page 6 of 36

Page 7 of 36

Environmental Science & Technology

121

statistical analysis and post hoc Tukey’s test were done to determine which group had higher

122

MIC values, as shown in the supporting information. For all analyses, the least square mean

123

graphical representation was plotted with Rstudio.

124

A fourth analysis involved 735 MIC values, but the MIC values were divided into two

125

groups: minimum and rich media so that the ‘media’ represented a categorical parameter. The

126

ANOVA statistical analysis and post hoc Tukey’s test were done to determine which group had

127

higher MIC values.

128

A fifth analysis involved the same 735 MIC values, but the MIC values were divided into

129

two groups: pure cultures and consortia so that the ‘biosorbent type’ represented a categorical

130

parameter. The ANOVA statistical analysis and post hoc Tukey’s test were done to determine

131

which group had higher MIC values.

132

Analysis of Microbial Maximum Sorption Capacity relationship to microbial kingdom and

133

biosorbent type

134

First, the relationship of the maximum sorption capacity, qmax, to the microbial kingdom was

135

investigated with qmax values for various heavy metals from 195 published studies. The

136

‘Kingdom’ (Eubacteria, Fungi, and Plantae) was used as a categorical parameter, whereas qmax

137

was used as a dependent parameter.

138

In a second analysis with 155 studies, the “metal” was used as a categorical parameter,

139

whereas the qmax was used as a dependent parameter. The data included MIC values of common

140

metals used in biosorption studies: Cd, Cr, Cu, Ni, Pb, and Zn only for the bacteria Kingdom.

141

A third analysis included using “biosorbent type” (pure cultures or consortia) as a categorical

142

parameter with the same 155 studies (97 for pure cultures and 58 for consortia from the bacteria 7 ACS Paragon Plus Environment

Environmental Science & Technology

143

Kingdom). These values were sorted into two main groups: Pure Cultures (PC) and Consortia

144

(C). (Table 1).

145

All consortia studies utilized in this analysis were a complex mixture of microorganisms

146

obtained from environmental samples (e.g. soil, water or wastewater) grown in the laboratory

147

with minimum media under aerobic conditions. None of the consortia studies were done in the

148

study site.

149

metals are present. The qmax values were calculated by the authors of each study. A few studies

150

had only sorption capacity values, which were used from the highest reported observed values, or

151

the maximum metal concentrations observed to be adsorbed, see Supporting Information. A

152

natural logarithm transformation of qmax values was done to obtain a normal distribution of all

153

of the data. The ANOVA statistical analysis and the post hoc Tukey’s test with Rstudio were

154

done for the three analyses to determine which group had higher sorption capacity values, and

155

the least square mean graphical representation was exported from Rstudio.

156

Most of the qmax values were obtained from Langmuir isotherm data where excess

3. Results and Discussion

157

3.1 Relationships among microbial kingdoms, bacterial genera, heavy metal tolerance, and

158

bioremediation capability

159

Microorganisms can differ in metal resistance and in their ability to remove heavy metals. In

160

the scientific literature, diverse microorganisms from the Eubacteria, Fungi, and Plantae

161

Kingdoms have shown evidence of heavy metal resistance. Within such Kingdoms, though,

162

some metal-resistant microorganisms have never been investigated for heavy metal remediation

163

capability.

164

considering their remediation capability, to understand whether a particular Kingdom is more

165

tolerant to heavy metals than others. Additionally, we also investigated the tolerance of different

9,10

Thus, we first compared the MIC of different microbial Kingdoms, without

8 ACS Paragon Plus Environment

Page 8 of 36

Page 9 of 36

Environmental Science & Technology

166

Eubacterial genera to determine whether different genera can have different metal tolerances. We

167

selected Eubacteria as a representative group for genus investigation since it is the most studied

168

Kingdom in the literature. The next step of our evaluation was to compare the remediation

169

capability of these Kingdoms in terms of metal sorption capacity. These results allowed us to

170

determine (i) whether heavy metal tolerance is intrinsic to any particular microbial Kingdom; (ii)

171

more specifically, whether the metal tolerance depends on the type of genus, and (iii) whether

172

microorganisms from a particular Kingdom that are tolerant to metals can play a significant role

173

in metal sorption capacity and hold bioremedation capabilities.

174

Relationship between microbial metal tolerance and microbial Kingdom

175

The relationship between microbial metal tolerance and Kingdom is key to determine the

176

types of microorganisms that can survive in environments contaminated with heavy metals and

177

potentially play a role in bioremediation processes. It is important, however, to first understand

178

whether microbial metal tolerance is related to the type of metal since different metals have

179

different redox capabilities, solubilities in water, and toxicity mechanisms under aerobic

180

conditions. The analysis presented in Figure 1 shows that there is a statistically significant

181

difference between the different metals and the overall microbial tolerance under the same redox

182

conditions (aerobic), with a p-value 0.01),

186

but are significantly different from As, Ni, Pb and Zn (Tukey’s test p0.01), but are

9 ACS Paragon Plus Environment

Environmental Science & Technology

189

significantly different from As and Pb (Tukey’s test p0.01), but are significantly different from

192

the rest of the metals (Tukey’s test p Zn > Cd > Cu.68 The uptake of

453

metals by yeast

454

extracellular materials produced by yeasts.14

455

3.2. Role of Biodiversity on Metal Tolerance and Sorption Capacity

has been attributed to intracellular sequestration and by the presence of

456

All the studies analyzed in the previous sections included only pure cultures. Although pure

457

cultures can have multiple metal resistance mechanisms, consortia can perform complicated

458

functions that individual populations cannot.70 Consortia can also be more robust to

459

environmental fluctuations, such as metal concentrations.70 Therefore, complex microbial

460

communities are typically more attractive for large-scale processes and for in situ

461

bioremediation.

462

tolerance, and sorption capacity. For that purpose, we will compare results from studies with

463

consortia, which contain multiple microbial species with various mechanisms of metal

464

resistance, with results from studies with pure cultures. This approach will allow us to determine

465

whether complex microbial communities are better at tolerating and removing heavy metals than

466

pure cultures.

467

Relationship between diversity and metal tolerance

In this study, we aim to establish relationships among biodiversity, metal

23 ACS Paragon Plus Environment

Environmental Science & Technology

468

The best way to determine whether microbial communities are more tolerant to metals than

469

pure cultures is to perform an analysis comparing microbial metal resistance between consortia

470

and pure cultures. Consortia in the present study represent communities of microorganisms

471

found in heavy metal contaminated environments that were grown in the laboratory in synthetic

472

minimum growth media prior to experimentation (e.g. MIC and sorption).

473

The relationship between microbial metal resistance and biodiversity is critical to understand

474

whether microbial diversity influences the mechanisms of metal tolerance. Figure 6 indicates

475

that there is a statistically significant difference between the two groups, with a p < 0.001

476

confidence level. The confidence level suggests that, on average, consortia have higher heavy

477

metal resistance. The higher metal resistance of consortia may be explained by the effective

478

communication between the microbial cells among different species. 91 Through communication

479

between cells, microbial consortia can trigger changes in gene expression in response to high

480

levels of metals. 71 The response to metal concentrations may happen by metabolic variations in

481

several community members, shifting the concentration and fate of dissolved metabolites, to

482

increase the tolerance for metals. 72

483

24 ACS Paragon Plus Environment

Page 24 of 36

Page 25 of 36

Environmental Science & Technology

484 485 486

Figure 6- Microbial metal resistance, expressed as the minimum inhibitory concentration, as a function of the biosorbent type. ANOVA results from 735 literature studies. Current effect: F(1,724)= 20.108, p