Ecogenomic responses of benthic communities under multiple stressors along the marine and adjacent riverine areas of northern Bohai Sea, China.

Benthic communities in the aquatic ecosystem are influenced by both natural and anthropogenic stressors. To understand the ecogenomic responses of sediment communities to the multiple stressors of polluted environments, the bacteria, protistan and metazoan communities in sediments from marine and adjacent riverine areas of North Bohai Sea were characterized by environmental DNA meta-systematics, and their associations with environmental variables were assessed by multiple statistical approaches. The bacterial communities were dominated by Firmicutes (mean 22.4%), Proteobacteria (mean 21.6%) and Actinobacteria (mean 21.5%). The protistan communities were dominated by Ochrophyta (33.7%), Cercozoa (18.9%) and Ciliophora (17.9%). Arthropoda (71.1%) dominated the metazoan communities in sediments. The structures of communities in sediments were shaped by both natural variables (spatial variability and/or salinity (presented as Na and Ca)) and anthropogenic contaminants, including DDTs, PAHs or metals (Cu, Al, Co, Cr, Cu, Fe, K, Mg, Mn, Ni and Zn). Particularly, the correlation network of multiple communities was modulated by the concentrations of Na and DDTs at the family level. Overall, environmental DNA meta-systematics can provide a powerful tool for biomonitoring, sediment quality assessment, and key stressors identification.

[1]  A. Morgan Sources and distribution of bay debris , 1993 .

[2]  I. Telesh,et al.  Life in the salinity gradient: Discovering mechanisms behind a new biodiversity pattern , 2013 .

[3]  R. Knight,et al.  Soil bacterial and fungal communities across a pH gradient in an arable soil , 2010, The ISME Journal.

[4]  J. Martiny,et al.  Microbial composition affects the functioning of estuarine sediments , 2012, The ISME Journal.

[5]  Yan-Li Lei,et al.  Distributions and Biomass of Benthic Ciliates, Foraminifera and Amoeboid Protists in Marine, Brackish, and Freshwater Sediments , 2014, The Journal of eukaryotic microbiology.

[6]  Luis Mauricio Bini,et al.  Mantel test in population genetics , 2013, Genetics and molecular biology.

[7]  Peter Zuber,et al.  Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient , 2011, The ISME Journal.

[8]  J. Giesy,et al.  Mercury in coastal watersheds along the Chinese Northern Bohai and Yellow Seas. , 2012, Journal of hazardous materials.

[9]  Stéphane Audic,et al.  The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy , 2012, Nucleic Acids Res..

[10]  M. Pusch,et al.  Comparison of bacterial production in sediments, epiphyton and the pelagic zone of a lowland river , 2001 .

[11]  J. Giesy,et al.  Ecological risk assessment of arsenic and metals in sediments of coastal areas of northern Bohai and Yellow Seas, China , 2010, AMBIO.

[12]  H. Ducklow Microbial services: challenges for microbial ecologists in a changing world , 2008 .

[13]  Philip Hugenholtz,et al.  Shining a Light on Dark Sequencing: Characterising Errors in Ion Torrent PGM Data , 2013, PLoS Comput. Biol..

[14]  Eske Willerslev,et al.  Environmental DNA - An emerging tool in conservation for monitoring past and present biodiversity , 2015 .

[15]  Paul D. Jones,et al.  Sources and distribution of polychlorinated-dibenzo-p-dioxins and -dibenzofurans in soil and sediment from the Yellow Sea region of China and Korea. , 2011, Environmental pollution.

[16]  Kalyan C. Mynampati,et al.  Ecogenomics reveals metals and land-use pressures on microbial communities in the waterways of a megacity. , 2015, Environmental science & technology.

[17]  Michel Coste,et al.  Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity. , 2010, The Science of the total environment.

[18]  E. Buskey,et al.  Toxicity of dispersant Corexit 9500A and crude oil to marine microzooplankton. , 2014, Ecotoxicology and environmental safety.

[19]  M. F. Dias,et al.  Impact of inocula and operating conditions on the microbial community structure of two anammox reactors , 2014, Environmental technology.

[20]  K. Fent Ecotoxicological problems associated with contaminated sites. , 2003, Toxicology letters.

[21]  A. Covich,et al.  Global Change and the Biodiversity of Freshwater Ecosystems: Impacts on Linkages between Above-Sediment and Sediment Biota , 2000, BioScience.

[22]  E. Long Ranges in chemical concentrations in sediments associated with adverse biological effects , 1992 .

[23]  V. Ranwez,et al.  A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents , 2013, Frontiers in Zoology.

[24]  D. Kirchman,et al.  Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient , 2012, The ISME Journal.

[25]  R. Schwarzenbach,et al.  The Challenge of Micropollutants in Aquatic Systems , 2006, Science.

[26]  M. Brinke,et al.  Effects of heavy metals on free-living nematodes: A multifaceted approach using growth, reproduction and behavioural assays , 2014 .

[27]  J. Giesy,et al.  PAHs in surface sediments from coastal and estuarine areas of the northern Bohai and Yellow Seas, China , 2012, Environmental Geochemistry and Health.

[28]  W. Manz,et al.  Anthropogenic pollutants affect ecosystem services of freshwater sediments: the need for a “triad plus x” approach , 2011 .

[29]  C. Berney,et al.  Cultivation-independent analysis reveals a shift in ciliate 18S rRNA gene diversity in a polycyclic aromatic hydrocarbon-polluted soil. , 2007, FEMS Microbiology Ecology.

[30]  R. Wagemann,et al.  Metal Toxicity to Algae: A Highly pH Dependent Phenomenon , 1984 .

[31]  R. Mendel,et al.  Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). , 2009, Current opinion in plant biology.

[32]  W. Norwood,et al.  Implications of Cu and Ni toxicity in two members of the Hyalella azteca cryptic species complex: Mortality, growth, and bioaccumulation parameters , 2016, Environmental toxicology and chemistry.

[33]  Mehrdad Hajibabaei,et al.  Simultaneous assessment of the macrobiome and microbiome in a bulk sample of tropical arthropods through DNA metasystematics , 2014, Proceedings of the National Academy of Sciences.

[34]  W. Traunspurger,et al.  The functional response of a freshwater benthic community to cadmium pollution. , 2012, Environmental pollution.

[35]  V. de Lorenzo,et al.  Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. , 2002, FEMS microbiology reviews.

[36]  S. Ye,et al.  Assessment of heavy metal contamination in surface sediments of the west Guangdong coastal region, China. , 2016, Marine pollution bulletin.

[37]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[38]  P. Madoni,et al.  Acute toxicity of heavy metals towards freshwater ciliated protists. , 2006, Environmental pollution.

[39]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[40]  R. Lohmann,et al.  Comparing sediment equilibrium partitioning and passive sampling techniques to estimate benthic biota PCDD/F concentrations in Newark Bay, New Jersey (U.S.A.). , 2014, Environmental pollution.

[41]  Robert C. Edgar,et al.  UPARSE: highly accurate OTU sequences from microbial amplicon reads , 2013, Nature Methods.

[42]  M. Wainwright,et al.  Effects of heavy metals on enzyme synthesis in substrate-amended river sediments , 1982, European journal of applied microbiology and biotechnology.

[43]  J. Giesy,et al.  HCH and DDT in Sediments from Marine and Adjacent Riverine Areas of North Bohai Sea, China , 2010, Archives of environmental contamination and toxicology.

[44]  P. Wong,et al.  Toxicity of a Mixture of Metals on Freshwater Algae , 1978 .

[45]  Janet M. Thornton,et al.  Metal ions in biological catalysis: from enzyme databases to general principles , 2008, JBIC Journal of Biological Inorganic Chemistry.

[46]  M. Hoostal,et al.  Local adaptation of microbial communities to heavy metal stress in polluted sediments of Lake Erie. , 2008, FEMS microbiology ecology.

[47]  P. Deschamps,et al.  Complex communities of small protists and unexpected occurrence of typical marine lineages in shallow freshwater systems. , 2015, Environmental microbiology.

[48]  Susan M. Huse,et al.  A Method for Studying Protistan Diversity Using Massively Parallel Sequencing of V9 Hypervariable Regions of Small-Subunit Ribosomal RNA Genes , 2009, PloS one.

[49]  J. Giesy,et al.  Using in situ bacterial communities to monitor contaminants in river sediments. , 2016, Environmental pollution.

[50]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Yonglong Lu,et al.  Environmental concentrations and bioaccumulations of cadmium and zinc in coastal watersheds along the Chinese Northern Bohai and Yellow Seas , 2013, Environmental toxicology and chemistry.

[52]  D. Persaud,et al.  Guidelines for the protection and management of aquatic sediment quality in Ontario , 1993 .

[53]  D. Gillan,et al.  Adherent bacteria in heavy metal contaminated marine sediments , 2007, Biofouling.

[54]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[55]  Jonathan Friedman,et al.  Inferring Correlation Networks from Genomic Survey Data , 2012, PLoS Comput. Biol..

[56]  Mark V Brown,et al.  Core sediment bacteria drive community response to anthropogenic contamination over multiple environmental gradients. , 2013, Environmental microbiology.

[57]  J. Claverie,et al.  Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing. , 2015, Environmental microbiology.

[58]  Anders F. Andersson,et al.  Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea , 2011, The ISME Journal.

[59]  M. Grote,et al.  Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale , 2014, Proceedings of the National Academy of Sciences.

[60]  S. Agustí,et al.  Polycyclic aromatic hydrocarbons alter the structure of oceanic and oligotrophic microbial food webs. , 2015, Marine pollution bulletin.

[61]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.