Impacts of Human Activities on the Composition and Abundance of Sulfate-Reducing and Sulfur-Oxidizing Microorganisms in Polluted River Sediments

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Abstract

Water system degradation has a severe impact on daily life, especially in developing countries. However, microbial changes associated with this degradation, especially changes in microbes related to sulfur (S) cycling, are poorly understood. In this study, the abundance, structure, and diversity of sulfate-reducing microorganisms (SRM) and sulfur-oxidizing microorganisms (SOM) in the sediments from the Ziya River Basin, which is polluted by various human interventions (urban and agricultural activities), were investigated. Quantitative real-time PCR showed that the S cycling-related (SCR) genes ( dsrB and soxB) were significantly elevated, reaching 2.60 × 10 ⁷ and 1.81 × 10 ⁸ copies per gram of dry sediment, respectively, in the region polluted by human urban activities (RU), and the ratio of dsrB to soxB abundance was significantly elevated in the region polluted by human agricultural activities (RA) compared with those in the protected wildlife reserve (RP), indicating that the mechanisms underlying water system degradation differ between RU and RA. Based on a 16S rRNA gene analysis, human interventions had substantial effects on microbial communities, particularly for microbes involved in S cycling. Some SCR genera (i.e., Desulfatiglans and Geothermobacter) were enriched in the sediments from both RA and RU, while others (i.e., Desulfofustis and Desulfonatronobacter) were only enriched in the sediments from RA. A redundancy analysis indicated that NH ₄ ⁺-N and total organic carbon significantly influenced the abundance of SRM and SOM, and sulfate significantly influenced only the abundance of SRM. A network analysis showed high correlation between SCR microorganisms and other microbial groups for both RU and RA, including those involved in carbon and metal cycling. These findings indicated the different effects of different human interventions on the microbial community composition and water quality degradation.

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Most cited references 55

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FLASH: fast length adjustment of short reads to improve genome assemblies.

T. Magoc, S. L. Salzberg (2013)

Next-generation sequencing technologies generate very large numbers of short reads. Even with very deep genome coverage, short read lengths cause problems in de novo assemblies. The use of paired-end libraries with a fragment size shorter than twice the read length provides an opportunity to generate much longer reads by overlapping and merging read pairs before assembling a genome. We present FLASH, a fast computational tool to extend the length of short reads by overlapping paired-end reads from fragment libraries that are sufficiently short. We tested the correctness of the tool on one million simulated read pairs, and we then applied it as a pre-processor for genome assemblies of Illumina reads from the bacterium Staphylococcus aureus and human chromosome 14. FLASH correctly extended and merged reads >99% of the time on simulated reads with an error rate of <1%. With adequately set parameters, FLASH correctly merged reads over 90% of the time even when the reads contained up to 5% errors. When FLASH was used to extend reads prior to assembly, the resulting assemblies had substantially greater N50 lengths for both contigs and scaffolds. The FLASH system is implemented in C and is freely available as open-source code at http://www.cbcb.umd.edu/software/flash. t.magoc@gmail.com.

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Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays.

M T Suzuki, L. T. Taylor, E F Delong (2000)

Few techniques are currently available for quantifying specific prokaryotic taxa in environmental samples. Quantification of specific genotypes has relied mainly on oligonucleotide hybridization to extracted rRNA or intact rRNA in whole cells. However, low abundance and cellular rRNA content limit the application of these techniques in aquatic environments. In this study, we applied a newly developed quantitative PCR assay (5'-nuclease assay, also known as TaqMan) to quantify specific small-subunit (SSU) rRNA genes (rDNAs) from uncultivated planktonic prokaryotes in Monterey Bay. Primer and probe combinations for quantification of SSU rDNAs at the domain and group levels were developed and tested for specificity and quantitative reliability. We examined the spatial and temporal variations of SSU rDNAs from Synechococcus plus Prochlorococcus and marine Archaea and compared the results of the quantitative PCR assays to those obtained by alternative methods. The 5'-nuclease assays reliably quantified rDNAs over at least 4 orders of magnitude and accurately measured the proportions of genes in artificial mixtures. The spatial and temporal distributions of planktonic microbial groups measured by the 5'-nuclease assays were similar to the distributions estimated by quantitative oligonucleotide probe hybridization, whole-cell hybridization assays, and flow cytometry.

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Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments.

G. Muyzer, A. Teske, C O Wirsen … (1995)

Denaturing gradient gel electrophoresis (DGGE) of PCR-amplified 16S rDNA fragments was used to explore the genetic diversity of hydrothermal vent microbial communities, specifically to determine the importance of sulfur-oxidizing bacteria therein. DGGE analysis of two different hydrothermal vent samples revealed one PCR band for one sample and three PCR bands for the other sample, which probably correspond to the dominant bacterial populations in these communities. Three of the four 16S rDNA fragments were sequenced. By comparison with 16S rRNA sequences of the Ribosomal Database Project, two of the DGGE-separated fragments were assigned to the genus Thiomicrospira. To identify these 'phylotypes' in more detail, a phylogenetic framework was created by determining the nearly complete 16S rRNA gene sequence (approx. 1500 nucleotides) from three described Thiomicrospira species, viz., Tms. crunogena, Tms. pelophila, Tms. denitrificans, and from a new isolate, Thiomicrospira sp. strain MA2-6. All Thiomicrospira species except Tms. denitrificans formed a monophyletic group within the gamma subdivision of the Proteobacteria. Tms. denitrificans was assigned as a member of the epsilon subdivision and was distantly affiliated with Thiovulum, another sulfur-oxidizing bacterium. Sequences of two dominant 16S rDNA fragments obtained by DGGE analysis fell into the gamma subdivision Thiomicrospira. The sequence of one fragment was in all comparable positions identical to the 16S rRNA sequence of Tms. crunogena. Identifying a dominant molecular isolate as Tms. crunogena indicates that this species is a dominant community member of hydrothermal vent sites. Another 'phylotype' represented a new Thiomicrospira species, phylogenetically in an intermediate position between Tms. crunogena and Tms. pelophila. The third 'phylotype' was identified as a Desulfovibrio, indicating that sulfate-reducing bacteria, as sources of sulfide, may complement sulfur- and sulfide-oxidizing bacteria ecologically in these sulfide-producing hydrothermal vents.

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Author and article information

Contributors

Rui Wang: URI : http://loop.frontiersin.org/people/569811/overview

Shengjun Xu: URI : http://loop.frontiersin.org/people/433110/overview

Cancan Jiang: URI : http://loop.frontiersin.org/people/569819/overview

Yang Zhang: URI : http://loop.frontiersin.org/people/569512/overview

Na Bai: URI : http://loop.frontiersin.org/people/569600/overview

Guoqiang Zhuang: URI : http://loop.frontiersin.org/people/433647/overview

Zhihui Bai: URI : http://loop.frontiersin.org/people/101737/overview

Xuliang Zhuang: URI : http://loop.frontiersin.org/people/432477/overview

Journal

Journal ID (nlm-ta): Front Microbiol

Journal ID (iso-abbrev): Front Microbiol

Journal ID (publisher-id): Front. Microbiol.

Title: Frontiers in Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-302X

Publication date (Electronic): 12 February 2019

Publication date Collection: 2019

Volume: 10

Electronic Location Identifier: 231

Affiliations

[1] ¹Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences , Beijing, China

[2] ²College of Resources and Environment, University of Chinese Academy of Sciences , Beijing, China

[3] ³School of Safety and Environmental Engineering, Capital University of Economics and Business , Beijing, China

Author notes

Edited by: Jonathan P. Zehr, University of California, Santa Cruz, United States

Reviewed by: Beverly E. Flood, University of Minnesota Twin Cities, United States; Sonja Kristine Fagervold, UMS2348 Observatoire Océanologique de Banyuls-sur-Mer (OOB), France

*Correspondence: Shengjun Xu, sjxu@ 123456rcees.ac.cn Xuliang Zhuang, xlzhuang@ 123456rcees.ac.cn

This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology

Article

DOI: 10.3389/fmicb.2019.00231

PMC ID: 6379298

PubMed ID: 30809217

SO-VID: e024f168-d3f8-4aa9-a18f-f0a1e873d2aa

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 15 June 2018

Date accepted : 28 January 2019

Page count

Figures: 4, Tables: 2, Equations: 0, References: 65, Pages: 13, Words: 0

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Impacts of Human Activities on the Composition and Abundance of Sulfate-Reducing and Sulfur-Oxidizing Microorganisms in Polluted River Sediments

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Most cited references 55

FLASH: fast length adjustment of short reads to improve genome assemblies.

Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays.

Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments.

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