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Title: Freshwater carbon and nutrient cycles revealed through reconstructed population genomes

Abstract

Although microbes mediate much of the biogeochemical cycling in freshwater, the categories of carbon and nutrients currently used in models of freshwater biogeochemical cycling are too broad to be relevant on a microbial scale. One way to improve these models is to incorporate microbial data. Here, we analyze both genes and genomes from three metagenomic time series and propose specific roles for microbial taxa in freshwater biogeochemical cycles. Our metagenomic time series span multiple years and originate from a eutrophic lake (Lake Mendota) and a humic lake (Trout Bog Lake) with contrasting water chemistry. Our analysis highlights the role of polyamines in the nitrogen cycle, the diversity of diazotrophs between lake types, the balance of assimilatory vs. dissimilatory sulfate reduction in freshwater, the various associations between types of phototrophy and carbon fixation, and the density and diversity of glycoside hydrolases in freshwater microbes. We also investigated aspects of central metabolism such as hydrogen metabolism, oxidative phosphorylation, methylotrophy, and sugar degradation. Finally, by analyzing the dynamics over time in nitrogen fixation genes and Cyanobacteria genomes, we show that the potential for nitrogen fixation is linked to specific populations in Lake Mendota. This work represents an important step towards incorporating microbial datamore » into ecosystem models and provides a better understanding of how microbes may participate in freshwater biogeochemical cycling.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1];  [1]; ORCiD logo [1];  [2];  [3];  [1]
  1. Univ. of Wisconsin-Madison, Madison, WI (United States)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Uppsala Univ., Uppsala (Sweden)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1510750
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PeerJ
Additional Journal Information:
Journal Volume: 6; Journal Issue: 12; Journal ID: ISSN 2167-8359
Publisher:
PeerJ Inc.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; Freshwater; Metabolism; Carbon cycling; Nutrient cycling; Microbial communities

Citation Formats

Linz, Alexandra M., He, Shaomei, Stevens, Sarah L. R., Anantharaman, Karthik, Rohwer, Robin R., Malmstrom, Rex R., Bertilsson, Stefan, and McMahon, Katherine D. Freshwater carbon and nutrient cycles revealed through reconstructed population genomes. United States: N. p., 2018. Web. doi:10.7717/peerj.6075.
Linz, Alexandra M., He, Shaomei, Stevens, Sarah L. R., Anantharaman, Karthik, Rohwer, Robin R., Malmstrom, Rex R., Bertilsson, Stefan, & McMahon, Katherine D. Freshwater carbon and nutrient cycles revealed through reconstructed population genomes. United States. doi:10.7717/peerj.6075.
Linz, Alexandra M., He, Shaomei, Stevens, Sarah L. R., Anantharaman, Karthik, Rohwer, Robin R., Malmstrom, Rex R., Bertilsson, Stefan, and McMahon, Katherine D. Mon . "Freshwater carbon and nutrient cycles revealed through reconstructed population genomes". United States. doi:10.7717/peerj.6075. https://www.osti.gov/servlets/purl/1510750.
@article{osti_1510750,
title = {Freshwater carbon and nutrient cycles revealed through reconstructed population genomes},
author = {Linz, Alexandra M. and He, Shaomei and Stevens, Sarah L. R. and Anantharaman, Karthik and Rohwer, Robin R. and Malmstrom, Rex R. and Bertilsson, Stefan and McMahon, Katherine D.},
abstractNote = {Although microbes mediate much of the biogeochemical cycling in freshwater, the categories of carbon and nutrients currently used in models of freshwater biogeochemical cycling are too broad to be relevant on a microbial scale. One way to improve these models is to incorporate microbial data. Here, we analyze both genes and genomes from three metagenomic time series and propose specific roles for microbial taxa in freshwater biogeochemical cycles. Our metagenomic time series span multiple years and originate from a eutrophic lake (Lake Mendota) and a humic lake (Trout Bog Lake) with contrasting water chemistry. Our analysis highlights the role of polyamines in the nitrogen cycle, the diversity of diazotrophs between lake types, the balance of assimilatory vs. dissimilatory sulfate reduction in freshwater, the various associations between types of phototrophy and carbon fixation, and the density and diversity of glycoside hydrolases in freshwater microbes. We also investigated aspects of central metabolism such as hydrogen metabolism, oxidative phosphorylation, methylotrophy, and sugar degradation. Finally, by analyzing the dynamics over time in nitrogen fixation genes and Cyanobacteria genomes, we show that the potential for nitrogen fixation is linked to specific populations in Lake Mendota. This work represents an important step towards incorporating microbial data into ecosystem models and provides a better understanding of how microbes may participate in freshwater biogeochemical cycling.},
doi = {10.7717/peerj.6075},
journal = {PeerJ},
issn = {2167-8359},
number = 12,
volume = 6,
place = {United States},
year = {2018},
month = {12}
}

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Works referenced in this record:

Polyamine transport in bacteria and yeast
journal, December 1999

  • Igarashi, Kazuei; Kashiwagi, Keiko
  • Biochemical Journal, Vol. 344, Issue 3
  • DOI: 10.1042/bj3440633

Genomes of Novel Microbial Lineages Assembled from the Sub-Ice Waters of Lake Baikal
journal, October 2017

  • Cabello-Yeves, Pedro J.; Zemskaya, Tamara I.; Rosselli, Riccardo
  • Applied and Environmental Microbiology, Vol. 84, Issue 1
  • DOI: 10.1128/AEM.02132-17

Ananke: temporal clustering reveals ecological dynamics of microbial communities
journal, January 2017

  • Hall, Michael W.; Rohwer, Robin R.; Perrie, Jonathan
  • PeerJ, Vol. 5
  • DOI: 10.7717/peerj.3812

Green sulphur bacteria as a component of the photosynthetic plankton community in small dimictic humic lakes with an anoxic hypolimnion
journal, March 2013

  • Karhunen, J.; Arvola, L.; Peura, S.
  • Aquatic Microbial Ecology, Vol. 68, Issue 3
  • DOI: 10.3354/ame01620

Both Forward and Reverse TCA Cycles Operate in Green Sulfur Bacteria
journal, July 2010

  • Tang, Kuo-Hsiang; Blankenship, Robert E.
  • Journal of Biological Chemistry, Vol. 285, Issue 46
  • DOI: 10.1074/jbc.M110.157834

Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006

  • DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
  • DOI: 10.1128/AEM.03006-05

Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
journal, August 2017

  • Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas
  • Nature Biotechnology, Vol. 35, Issue 8
  • DOI: 10.1038/nbt.3893

Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
journal, August 2017


Whole-lake mineralization of allochthonous and autochthonous organic carbon in a large humic lake (örträsket, N. Sweden)
journal, November 2001

  • Jonsson, Anders; Meili, Markus; Bergström, Ann-Kristin
  • Limnology and Oceanography, Vol. 46, Issue 7
  • DOI: 10.4319/lo.2001.46.7.1691

dbCAN2: a meta server for automated carbohydrate-active enzyme annotation
journal, May 2018

  • Zhang, Han; Yohe, Tanner; Huang, Le
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky418

[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation
journal, June 2015

  • Peters, John W.; Schut, Gerrit J.; Boyd, Eric S.
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6
  • DOI: 10.1016/j.bbamcr.2014.11.021

Interannual dynamics and phenology of bacterial communities in a eutrophic lake
journal, March 2007

  • Shade, Ashley; Kent, Angela D.; Jones, Stuart E.
  • Limnology and Oceanography, Vol. 52, Issue 2
  • DOI: 10.4319/lo.2007.52.2.0487

Lakes and streams as sentinels of environmental change in terrestrial and atmospheric processes
journal, June 2008

  • Williamson, Craig E.; Dodds, Walter; Kratz, Timothy K.
  • Frontiers in Ecology and the Environment, Vol. 6, Issue 5
  • DOI: 10.1890/070140

Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes
journal, December 2004


Distinct and diverse anaerobic bacterial communities in boreal lakes dominated by candidate division OD1
journal, March 2012

  • Peura, Sari; Eiler, Alexander; Bertilsson, Stefan
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.21

The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign
journal, May 2015

  • Salcher, Michaela M.; Neuenschwander, Stefan M.; Posch, Thomas
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.55

FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Methylotrophy in Methylobacterium extorquens AM1 from a Genomic Point of View
journal, May 2003


Algae–bacteria interactions: Evolution, ecology and emerging applications
journal, January 2016


A Guide to the Natural History of Freshwater Lake Bacteria
journal, March 2011

  • Newton, R. J.; Jones, S. E.; Eiler, A.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1
  • DOI: 10.1128/MMBR.00028-10

Minimus: a fast, lightweight genome assembler
journal, January 2007

  • Sommer, Daniel D.; Delcher, Arthur L.; Salzberg, Steven L.
  • BMC Bioinformatics, Vol. 8, Issue 1
  • DOI: 10.1186/1471-2105-8-64

The Role of Nitrogen Fixation in Cyanobacterial Bloom Toxicity in a Temperate, Eutrophic Lake
journal, February 2013


IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake
journal, December 2012

  • Salcher, Michaela M.; Posch, Thomas; Pernthaler, Jakob
  • The ISME Journal, Vol. 7, Issue 5
  • DOI: 10.1038/ismej.2012.162

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015


Investigation of XoxF methanol dehydrogenases reveals new methylotrophic bacteria in pelagic marine and freshwater ecosystems
journal, August 2015

  • Ramachandran, Arthi; Walsh, David A.
  • FEMS Microbiology Ecology, Vol. 91, Issue 10
  • DOI: 10.1093/femsec/fiv105

Autochthonous versus allochthonous carbon sources of bacteria: Results from whole-lake 13 C addition experiments
journal, March 2004

  • Kritzberg, Emma S.; Cole, Jonathan J.; Pace, Michael L.
  • Limnology and Oceanography, Vol. 49, Issue 2
  • DOI: 10.4319/lo.2004.49.2.0588

Microbial species delineation using whole genome sequences
journal, July 2015

  • Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
  • Nucleic Acids Research, Vol. 43, Issue 14
  • DOI: 10.1093/nar/gkv657

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Fast and accurate long-read alignment with Burrows–Wheeler transform
journal, January 2010


FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


Reshaping Data with the reshape Package
journal, January 2007


Ray Meta: scalable de novo metagenome assembly and profiling
journal, January 2012

  • Boisvert, Sébastien; Raymond, Frédéric; Godzaridis, Élénie
  • Genome Biology, Vol. 13, Issue 12
  • DOI: 10.1186/gb-2012-13-12-r122

Metatranscriptomic signature of exogenous polyamine utilization by coastal bacterioplankton: Polyamine-transforming genes in marine bacterial communities
journal, September 2011


Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria
journal, January 2016

  • Eiler, Alexander; Mondav, Rhiannon; Sinclair, Lucas
  • The ISME Journal, Vol. 10, Issue 8
  • DOI: 10.1038/ismej.2015.260

Reconstructing the various facets of dissolved organic carbon bioavailability in freshwater ecosystems
journal, March 2011


Experimental factors affecting PCR-based estimates of microbial species richness and evenness
journal, January 2010

  • Engelbrektson, Anna; Kunin, Victor; Wrighton, Kelly C.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.153

Heterotrophic Bacterial Growth Efficiency and Community Structure at Different Natural Organic Carbon Concentrations
journal, July 2003


Plumbing the Global Carbon Cycle: Integrating Inland Waters into the Terrestrial Carbon Budget
journal, February 2007


Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
journal, September 2017


Metagenomic insights into strategies of aerobic and anaerobic carbon and nitrogen transformation in boreal lakes
journal, July 2015

  • Peura, Sari; Sinclair, Lucas; Bertilsson, Stefan
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep12102

Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia
journal, April 2012


VSEARCH: a versatile open source tool for metagenomics
journal, January 2016


Microcystin mcyA and mcyE Gene Abundances Are Not Appropriate Indicators of Microcystin Concentrations in Lakes
journal, May 2015


Molecular Characterization of Methanotrophic Isolates from Freshwater Lake Sediment
journal, December 2000


Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics
journal, October 2017


Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system
journal, January 2011


SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler
journal, December 2012


Biogenic Amines in Fish: Roles in Intoxication, Spoilage, and Nitrosamine Formation—A Review
journal, February 2009

  • Bulushi, Ismail Al; Poole, Susan; Deeth, Hilton C.
  • Critical Reviews in Food Science and Nutrition, Vol. 49, Issue 4
  • DOI: 10.1080/10408390802067514

Polymeric and free sugars released by three phytoplanktonic species from a freshwater tropical eutrophic reservoir
journal, July 2005

  • Giroldo, Danilo; Vieira, Armando Augusto Henriques
  • Journal of Plankton Research, Vol. 27, Issue 7
  • DOI: 10.1093/plankt/fbi043

TaxAss: Leveraging a Custom Freshwater Database Achieves Fine-Scale Taxonomic Resolution
journal, September 2018


Aquatic carbon cycling in the conterminous United States and implications for terrestrial carbon accounting
journal, December 2015

  • Butman, David; Stackpoole, Sarah; Stets, Edward
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 1
  • DOI: 10.1073/pnas.1512651112

PhyloSift: phylogenetic analysis of genomes and metagenomes
journal, January 2014

  • Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.243

The Phylogenetic Position of the Family Methylococcaceae
journal, July 1995

  • Bowman, J. P.; Sly, L. I.; Stackebrandt, E.
  • International Journal of Systematic Bacteriology, Vol. 45, Issue 3
  • DOI: 10.1099/00207713-45-3-622a

Denitrification Across Landscapes and Waterscapes: a Synthesis
journal, December 2006


APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004


Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage
journal, August 2014

  • Ghylin, Trevor W.; Garcia, Sarahi L.; Moya, Francisco
  • The ISME Journal, Vol. 8, Issue 12
  • DOI: 10.1038/ismej.2014.135

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

  • Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13219

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Structural and sequence-based classification of glycoside hydrolases
journal, October 1997


Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Eutrophication of freshwater and coastal marine ecosystems a global problem
journal, March 2003


Whole-Genome Analysis of the Methyl tert-Butyl Ether-Degrading Beta-Proteobacterium Methylibium petroleiphilum PM1
journal, December 2006

  • Kane, S. R.; Chakicherla, A. Y.; Chain, P. S. G.
  • Journal of Bacteriology, Vol. 189, Issue 5
  • DOI: 10.1128/JB.01259-06

Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities
journal, May 2014


Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations
journal, January 2016

  • Bendall, Matthew L.; Stevens, Sarah LR; Chan, Leong-Keat
  • The ISME Journal, Vol. 10, Issue 7
  • DOI: 10.1038/ismej.2015.241

High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton
journal, June 2011

  • Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J.
  • The ISME Journal, Vol. 6, Issue 1
  • DOI: 10.1038/ismej.2011.84

Novel methylotrophic isolates from lake sediment, description of Methylotenera versatilis sp. nov. and emended description of the genus Methylotenera
journal, February 2011

  • Kalyuzhnaya, M. G.; Beck, D. A. C.; Vorobev, A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue 1
  • DOI: 10.1099/ijs.0.029165-0