Freshwater carbon and nutrient cycles revealed through reconstructed population genomes

Alexandra M Linz; Shaomei He; Sarah L R Stevens; Karthik Anantharaman; Robin R Rohwer; Rex R Malmstrom; Stefan Bertilsson; Katherine D McMahon

doi:10.7717/peerj.6075

Freshwater carbon and nutrient cycles revealed through reconstructed population genomes

PeerJ. 2018 Dec 10:6:e6075. doi: 10.7717/peerj.6075. eCollection 2018.

Authors

Alexandra M Linz¹, Shaomei He^{1

2}, Sarah L R Stevens¹, Karthik Anantharaman¹, Robin R Rohwer³, Rex R Malmstrom⁴, Stefan Bertilsson⁵, Katherine D McMahon^{1

6}

Affiliations

¹ Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, USA.
² Department of Geoscience, University of Wisconsin-Madison, Madison, WI, USA.
³ Environmental Chemistry and Technology Program, University of Wisconsin-Madison, Madison, WI, USA.
⁴ Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.
⁵ Department of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
⁶ Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.

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 data into ecosystem models and provides a better understanding of how microbes may participate in freshwater biogeochemical cycling.

Keywords: Carbon cycling; Freshwater; Metabolism; Microbial communities; Nutrient cycling.

Grants and funding

This research was supported by the U.S. Department of Energy Joint Genome Institute through the Community Sequencing Program (CSP 394). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. Katherine D. McMahon received funding from the United States National Science Foundation Microbial Observatories program (MCB-0702395), the Long Term Ecological Research Program (NTL–LTER DEB-1440297), and an INSPIRE award (DEB-1344254). Alexandra M. Linz was supported by a pre-doctoral fellowship provided by the University of Wisconsin–Madison Department of Bacteriology and by the National Science Foundation Graduate Research Fellowship Program under grant no. DGE-1256259 during this research. This material is also based upon work supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture (Hatch Project 1002996). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.