Spatial and temporal metagenomics of river compartments reveals viral community dynamics in an urban impacted stream

Although river ecosystems comprise less than 1% of Earth’s total non-glaciated area, they are critical modulators of microbially and virally orchestrated global biogeochemical cycles. However, most studies either use data that is not spatially resolved or is collected at timepoints that do not reflect the short life cycles of microorganisms. As a result, the relevance of microbiome interactions and the impacts they have over time on biogeochemical cycles are poorly understood. To assess how viral and microbial communities change over time, we sampled surface water and pore water compartments of the wastewater-impacted River Erpe in Germany every 3 hours over a 48-hour period resulting in 32 metagenomes paired to geochemical and metabolite measurements. We reconstructed 6,500 viral and 1,033 microbial genomes and found distinct communities associated with each river compartment. We show that 17% of our vMAGs clustered to viruses from other ecosystems like wastewater treatment plants and rivers. Our results also indicated that 70% of the viral community was persistent in surface waters, whereas only 13% were persistent in the pore waters taken from the hyporheic zone. Finally, we predicted linkages between 73 viral genomes and 38 microbial genomes. These putatively linked hosts included members of the Competibacteraceae, which we suggest are potential contributors to carbon and nitrogen cycling. Together, these findings demonstrate that microbial and viral communities in surface waters of this urban river can exist as stable communities along a flowing river; and raise important considerations for ecosystem models attempting to constrain dynamics of river biogeochemical cycles.

[1]  Yulin Wang,et al.  Genome-centric metagenomics reveals the host-driven dynamics and ecological role of CPR bacteria in an activated sludge system , 2023, Microbiome.

[2]  A. Vardi,et al.  Viral infection in the ocean—A journey across scales , 2023, PLoS biology.

[3]  Wenjun Li,et al.  Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts , 2022, Microbiome.

[4]  L. Deng,et al.  Insights into the global freshwater virome , 2022, Frontiers in Microbiology.

[5]  S. Kelly,et al.  Metabolic arsenal of giant viruses: Host hijack or self-use? , 2022, eLife.

[6]  B. Engelen,et al.  Auxiliary Metabolic Gene Functions in Pelagic and Benthic Viruses of the Baltic Sea , 2022, Frontiers in Microbiology.

[7]  Dehua Zhao,et al.  Effect of wastewater treatment plant discharge on the bacterial community in a receiving river. , 2022, Ecotoxicology and environmental safety.

[8]  N. Schuwirth,et al.  Wastewater microorganisms impact microbial diversity and important ecological functions of stream periphyton , 2022, bioRxiv.

[9]  Taeho Lee,et al.  Insight into impact of sewage discharge on microbial dynamics and pathogenicity in river ecosystem , 2022, Scientific reports.

[10]  Elizabeth K. Eder,et al.  Genome-Resolved Metaproteomics Decodes the Microbial and Viral Contributions to Coupled Carbon and Nitrogen Cycling in River Sediments , 2022, bioRxiv.

[11]  Dai Yamazaki,et al.  The importance of hydrology in routing terrestrial carbon to the atmosphere via global streams and rivers , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Meng Li,et al.  A mixed blessing of viruses in wastewater treatment plants. , 2022, Water research.

[13]  J. Jansson,et al.  Active virus-host interactions at sub-freezing temperatures in Arctic peat soil , 2021, Microbiome.

[14]  S. Deorowicz,et al.  PHIST: fast and accurate prediction of prokaryotic hosts from metagenomic viral sequences , 2021, bioRxiv.

[15]  M. Breitbart,et al.  Spatial and Temporal Dynamics of Prokaryotic and Viral Community Assemblages in a Lotic System (Manatee Springs, Florida) , 2021, Applied and environmental microbiology.

[16]  B. Poulter,et al.  Half of global methane emissions come from highly variable aquatic ecosystem sources , 2021, Nature Geoscience.

[17]  Jingjie Feng,et al.  Response of bacterial communities to variation in water quality and physicochemical conditions in a river-reservoir system , 2021 .

[18]  Anders F. Andersson,et al.  The Fennoscandian Shield deep terrestrial virosphere suggests slow motion ‘boom and burst’ cycles , 2021, Communications biology.

[19]  J. Lewandowski,et al.  Simultaneous attenuation of trace organics and change in organic matter composition in the hyporheic zone of urban streams , 2021, Scientific Reports.

[20]  Tom O. Delmont,et al.  VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses , 2021, Microbiome.

[21]  P. Tomalski,et al.  Relationships of Hydrological Seasons in Rivers and Groundwaters in Selected Catchments in Poland , 2021, Water.

[22]  Atul K. Jain,et al.  Global Carbon Budget 2020 , 2020, Earth System Science Data.

[23]  Xiaorui Song,et al.  Bacterial community structure upstream and downstream of cascade dams along the Lancang River in southwestern China , 2020, Environmental Science and Pollution Research.

[24]  M. Sullivan,et al.  DRAM for distilling microbial metabolism to automate the curation of microbiome function , 2020, bioRxiv.

[25]  M. Delgado‐Baquerizo,et al.  Soil Microbial Biogeography in a Changing World: Recent Advances and Future Perspectives , 2020, mSystems.

[26]  Joshua S Weitz,et al.  A Primer for Microbiome Time-Series Analysis , 2020, Frontiers in Genetics.

[27]  A. Arkin,et al.  Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity , 2020, Microbiome.

[28]  R. Malmstrom,et al.  Host population diversity as a driver of viral infection cycle in wild populations of green sulfur bacteria with long standing virus-host interactions , 2020, The ISME Journal.

[29]  A. Mushegian,et al.  Are There 1031 Virus Particles on Earth, or More, or Fewer? , 2020, Journal of bacteriology.

[30]  G. Bohrer,et al.  Methane and nitrous oxide porewater concentrations and surface fluxes of a regulated river. , 2020, The Science of the total environment.

[31]  Donovan H Parks,et al.  GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database , 2019, Bioinform..

[32]  K. Williams,et al.  Heterogeneity in Hyporheic Flow, Pore Water Chemistry, and Microbial Community Composition in an Alpine Streambed , 2019, Journal of Geophysical Research: Biogeosciences.

[33]  K. Konstantinidis,et al.  Prevalence of viral photosynthesis genes along a freshwater to saltwater transect in Southeast USA. , 2019, Environmental microbiology reports.

[34]  Evelien M. Adriaenssens,et al.  Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks , 2019, Nature Biotechnology.

[35]  Feng Li,et al.  MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies , 2019, PeerJ.

[36]  Natalia N. Ivanova,et al.  Minimum Information about an Uncultivated Virus Genome (MIUViG) , 2018, Nature Biotechnology.

[37]  James C. Stegen,et al.  WHONDRS: a Community Resource for Studying Dynamic River Corridors , 2018, mSystems.

[38]  T. Pavelsky,et al.  Global extent of rivers and streams , 2018, Science.

[39]  R. Milo,et al.  The biomass distribution on Earth , 2018, Proceedings of the National Academy of Sciences.

[40]  Arghavan Alisoltani,et al.  Metagenomic analysis of the bacterial communities and their functional profiles in water and sediments of the Apies River, South Africa, as a function of land use. , 2018, The Science of the total environment.

[41]  L. Paša-Tolić,et al.  Formularity: Software for Automated Formula Assignment of Natural and Other Organic Matter from Ultrahigh-Resolution Mass Spectra. , 2017, Analytical chemistry.

[42]  Neil D. Rawlings,et al.  The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database , 2017, Nucleic Acids Res..

[43]  Daniel J. Wilson,et al.  The distribution of bacterial doubling times in the wild , 2017, bioRxiv.

[44]  Rob Egan,et al.  Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics , 2017, Nature Communications.

[45]  W. Nelson,et al.  Geochemical and Microbial Community Attributes in Relation to Hyporheic Zone Geological Facies , 2017, Scientific Reports.

[46]  Michele Mauri,et al.  RAWGraphs: A Visualisation Platform to Create Open Outputs , 2017, CHItaly.

[47]  P. Forterre,et al.  Numerous cultivated and uncultivated viruses encode ribosomal proteins , 2017, bioRxiv.

[48]  Natalia N. Ivanova,et al.  Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea , 2017, Nature Biotechnology.

[49]  J. Banfield,et al.  dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication , 2017, The ISME Journal.

[50]  E. Graham,et al.  Deterministic influences exceed dispersal effects on hydrologically‐connected microbiomes , 2017, Environmental microbiology.

[51]  T. Northen,et al.  Dynamic substrate preferences predict metabolic properties of a simple microbial consortium , 2017, BMC Bioinformatics.

[52]  R. Dahlgren,et al.  Modeling nitrous oxide emission from rivers: a global assessment , 2016, Global change biology.

[53]  Yan Li,et al.  SeqKit: A Cross-Platform and Ultrafast Toolkit for FASTA/Q File Manipulation , 2016, PloS one.

[54]  B. Hurwitz,et al.  Viral metabolic reprogramming in marine ecosystems. , 2016, Current opinion in microbiology.

[55]  P. Videnska,et al.  Seasonal changes in microbial community composition in river water studied using 454-pyrosequencing , 2016, SpringerPlus.

[56]  Y. Rubin,et al.  Simulating bioclogging effects on dynamic riverbed permeability and infiltration , 2016 .

[57]  Luis Pedro Coelho,et al.  Plankton networks driving carbon export in the oligotrophic ocean , 2015, Nature.

[58]  T. Kruse,et al.  Impact of a wastewater treatment plant on microbial community composition and function in a hyporheic zone of a eutrophic river , 2015, Scientific Reports.

[59]  C. Suttle,et al.  Biogeography of Viruses in the Sea. , 2015, Annual review of virology.

[60]  Connor T. Skennerton,et al.  CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes , 2015, Genome research.

[61]  P. Peduzzi Virus ecology of fluvial systems: a blank spot on the map? , 2015, Biological reviews of the Cambridge Philosophical Society.

[62]  P. Bork,et al.  Patterns and ecological drivers of ocean viral communities , 2015, Science.

[63]  Michael J E Sternberg,et al.  The Phyre2 web portal for protein modeling, prediction and analysis , 2015, Nature Protocols.

[64]  Michael Springer,et al.  Natural Variation in Preparation for Nutrient Depletion Reveals a Cost–Benefit Tradeoff , 2014, bioRxiv.

[65]  Kunihiko Sadakane,et al.  MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph , 2014, Bioinform..

[66]  Bonnie L Hurwitz,et al.  Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome , 2014, The ISME Journal.

[67]  J. Balcázar,et al.  Use of pyrosequencing to explore the benthic bacterial community structure in a river impacted by wastewater treatment plant discharges. , 2014, Research in microbiology.

[68]  Karthik Anantharaman,et al.  Sulfur Oxidation Genes in Diverse Deep-Sea Viruses , 2014, Science.

[69]  Suchismita Ghosh,et al.  Impacts of Labile Organic Carbon Concentration on Organic and Inorganic Nitrogen Utilization by a Stream Biofilm Bacterial Community , 2013, Applied and Environmental Microbiology.

[70]  Connor T. Skennerton,et al.  Crass: identification and reconstruction of CRISPR from unassembled metagenomic data , 2013, Nucleic acids research.

[71]  M. Sullivan,et al.  Phylogenomics of T4 cyanophages: lateral gene transfer in the 'core' and origins of host genes. , 2012, Environmental microbiology.

[72]  J. Fuhrman,et al.  Seasonality and monthly dynamics of marine myovirus communities. , 2012, Environmental microbiology.

[73]  Siu-Ming Yiu,et al.  IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth , 2012, Bioinform..

[74]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[75]  S. Wilhelm,et al.  Viral and bacterial abundance and production in the Western Pacific Ocean and the relation to other oceanic realms. , 2012, FEMS microbiology ecology.

[76]  J. Lewandowski,et al.  Fate of organic micropollutants in the hyporheic zone of a eutrophic lowland stream: results of a preliminary field study. , 2011, The Science of the total environment.

[77]  R. Danovaro,et al.  Viral decay and viral production rates in continental-shelf and deep-sea sediments of the Mediterranean Sea. , 2010, FEMS microbiology ecology.

[78]  M. Robinson,et al.  A scaling normalization method for differential expression analysis of RNA-seq data , 2010, Genome Biology.

[79]  D. O’Donnell,et al.  The Effect of Municipal Wastewater Effluent on Nitrogen Levels in Onondaga Lake, a 36‐Year Record , 2010, Water environment research : a research publication of the Water Environment Federation.

[80]  S. Keleş,et al.  Sparse partial least squares regression for simultaneous dimension reduction and variable selection , 2010, Journal of the Royal Statistical Society. Series B, Statistical methodology.

[81]  Qing X. Li,et al.  Bacterial Degradation of Aromatic Compounds , 2009, International journal of environmental research and public health.

[82]  S. Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[83]  Y. Bettarel,et al.  Effects of freshwater and seawater mixing on virio- and bacterioplankton in a tropical estuary , 2008 .

[84]  P. Peduzzi,et al.  Viruses, bacteria and suspended particles in a backwater and main channel site of the Danube (Austria) , 2008, Aquatic Sciences.

[85]  C. Suttle Marine viruses — major players in the global ecosystem , 2007, Nature Reviews Microbiology.

[86]  Luke R. Thompson,et al.  Prevalence and Evolution of Core Photosystem II Genes in Marine Cyanobacterial Viruses and Their Hosts , 2006, PLoS biology.

[87]  C. Munn Viruses as pathogens of marine organisms—from bacteria to whales , 2006, Journal of the Marine Biological Association of the United Kingdom.

[88]  M. Weinbauer Ecology of prokaryotic viruses. , 2004, FEMS microbiology reviews.

[89]  M. Weinbauer,et al.  Are viruses driving microbial diversification and diversity? , 2003, Environmental microbiology.

[90]  J. Rosazza,et al.  GTP Cyclohydrolase I: Purification, Characterization, and Effects of Inhibition on Nitric Oxide Synthase in Nocardia Species , 2003, Applied and Environmental Microbiology.

[91]  Sunghwan Kim,et al.  Graphical method for analysis of ultrahigh-resolution broadband mass spectra of natural organic matter, the van Krevelen diagram. , 2003, Analytical chemistry.

[92]  Jessica D. Lundquist,et al.  Seasonal and Spatial Patterns in Diurnal Cycles in Streamflow in the Western United States , 2002 .

[93]  W. Dennison,et al.  Virus‐like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries , 2001 .

[94]  R. Hendrix,et al.  Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[95]  U. Uehlinger,et al.  Contribution of the Hyporheic Zone to Ecosystem Metabolism in a Prealpine Gravel-Bed-River , 1997, Journal of the North American Benthological Society.

[96]  W. Lammers Stimulation of bacterial cytokinesis by bacteriophage predation , 1992, Hydrobiologia.

[97]  R. Perry,et al.  THE ADSORPTION AND RELEASE OF PHOSPHATE FROM SEDIMENTS OF A RIVER RECEIVING SEWAGE EFFLUENT , 1989 .

[98]  J. Mcintosh Viruses , 1946 .

[99]  Alfonso Román,et al.  A graphical approach to characterize sub-daily flow regimes and evaluate its alterations due to hydropeaking. , 2017, The Science of the total environment.

[100]  M. Pusch,et al.  Community respiration in hyporheic sediments of a mountain stream (Steina, Black Forest) , 1994 .

[101]  P. Servais,et al.  Bacterioplankton in the Seine River (France): impact of the Parisian urban effluent , 1992 .

[102]  P. Bifani,et al.  Molecular Characterization of Mycobacterium tuberculosis H37Rv/Ra Variants: Distinguishing the Mycobacterial Laboratory Strain , 2000, Journal of Clinical Microbiology.