Response of Soil Microbial Communities to ... - ACS Publications

Jul 12, 2017 - Arsenic Contamination Indicates the Relationship between the .... located in eastern Dushan County, Guizhou Province, South- west China...
0 downloads 0 Views 2MB Size
Subscriber access provided by UNIV OF TEXAS ARLINGTON

Article

Response of soil microbial communities to elevated antimony and arsenic contamination indicates the relationship between the innate microbiota and contaminant fractions Weimin Sun, Enzong Xiao, Tangfu Xiao, Valdis Krumins, Qi Wang, Max M. Haggblom, Yiran Dong, Song Tang, Min Hu, Baoqin Li, Bingqing Xia, and Wei Liu Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b00294 • Publication Date (Web): 12 Jul 2017 Downloaded from http://pubs.acs.org on July 12, 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 38

Environmental Science & Technology

84x47mm (300 x 300 DPI)

ACS Paragon Plus Environment

Environmental Science & Technology

Page 2 of 38

1

Response of soil microbial communities to elevated antimony and arsenic

2

contamination indicates the relationship between the innate microbiota and

3

contaminant fractions

4

Weimin Sun1 , Enzong Xiao2,3,4 , Tangfu Xiao 2,3*, Valdis Krumins5, Qi Wang1, Max

5

Häggblom6, Yiran Dong7, Song Tang8, Min Hu1, Baoqin Li1, Bingqing Xia1,Wei Liu9

6

1. Guangdong Key Laboratory of Agricultural Environment Pollution Integrated





7

Control, Guangdong Institute of Eco-Environmental Science & Technology,

8

Guangzhou 510650, China

9

2. Key Laboratory of Water Quality and Conservation in the Pearl River Delta,

10

Ministry of Education, School of Environmental Science and Engineering,

11

Guangzhou University, Guangzhou 510006, China

12 13

3. State Key Laboratory of Environmental Geochemistry, Chinese Academy of Sciences, Guiyang 550081, China

14

4. University of Chinese Academy of Sciences, Beijing 100049, China.

15

5. Department of Environmental Sciences, Rutgers University, New Brunswick NJ

16 17 18 19 20

08901, USA 6. Department of Biochemistry and Microbiology, Rutgers University, New Brunswick NJ 08901, USA 7. Institute for Genomic Biology, University of Illinois, Urbana-Champaign, Urbana IL 61801, USA

1 ACS Paragon Plus Environment

Page 3 of 38

Environmental Science & Technology

21

8. National Institute of Environmental Health, Chinese Center for Disease Control

22

and Prevention, Beijing 100021, China Water Resources Protection Bureau of

23

Pearl River Water Resources Commission, Guangzhou 510611, China

24

*Corresponding author.

Mailing address: 99 Lincheng Road West, Guiyang 550081,

25

Guizhou Province, P. R. China. Phone: +86-851-85895318. Fax: +86-851-85891334. Email:

26

[email protected]

27

†These authors contributed equally to this work.

2 ACS Paragon Plus Environment

Environmental Science & Technology

Page 4 of 38

28

Abstract

29

Mining of sulfide ore deposits containing metalloids, such as antimony and arsenic,

30

has introduced serious soil contamination around the world, posing severe threats to

31

food safety and human health. Hence, it is important to understand the behavior and

32

composition of the microbial communities that control the mobilization or

33

sequestration of these metal(loid)s. Here, we selected two sites in Southwest China

34

with different levels of Sb and As contamination to study interactions among various

35

Sb and As fractions and the soil microbiota, with a focus on the microbial response to

36

metalloid contamination. Comprehensive geochemical analyses and 16S rRNA gene

37

amplicon sequencing demonstrated distinct soil taxonomic inventories depending on

38

Sb and As contamination levels. Stochastic gradient boosting indicated that citric acid

39

extractable Sb(V) and As(V) contributed 5% and 15%, respectively, to influencing the

40

community diversity. Random forest predicted that low concentrations of Sb(V) and

41

As(V) could enhance the community diversity but generally, the Sb and As

42

contamination impairs microbial diversity. Co-occurrence network analysis indicated

43

a strong correlation between the indigenous microbial communities and various Sb

44

and As fractions. A number of taxa were identified as core genera due to their

45

elevated abundances and positive correlation with contaminant fractions (total Sb and

46

As concentrations, bioavailable Sb and As extractable fractions, and Sb and As redox

47

species). Shotgun metagenomics indicated that Sb and As biogeochemical redox

48

reactions may exist in contaminated soils. All these observations suggest the potential

49

for bioremediation of Sb- and As-contaminated soils. 3 ACS Paragon Plus Environment

Page 5 of 38

Environmental Science & Technology

50

Keywords: Sb and As contaminated soil; Metagenomics; Stochastic gradient boosting;

51

Random forest; Co-occurrence network

52

53

Introduction

54

Antimony (Sb) and arsenic (As) are two toxic metalloids belonging to group 15 of the

55

Periodic Table. Both are suspected carcinogens and US EPA priority pollutants 1, 2. Sb

56

is widely distributed in the lithosphere and frequently associated with As in

57

sulfide-rich ores 3. Thus, co-contamination of Sb and As is commonly observed in

58

mining areas 4. The environmental toxicities of Sb and As are strongly dependent on

59

their redox species 5. For both, their reduced forms, i.e., Sb(III) and As(III), are more

60

toxic than their oxidized counterparts, (Sb(V) and As(V)) 6-8. In general, background

61

concentrations of Sb in soil are low (