Title: Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes

Abstract

Microbes are critical in carbon and nutrient cycling in freshwater ecosystems. Members of theVerrucomicrobiaare ubiquitous in such systems, and yet their roles and ecophysiology are not well understood. In this study, we recovered 19 Verrucomicrobia draft genomes by sequencing 184 time-series metagenomes from a eutrophic lake and a humic bog that differ in carbon source and nutrient availabilities. These genomes span four of the seven previously defined Verrucomicrobia subdivisions and greatly expand knowledge of the genomic diversity of freshwater Verrucomicrobia. Genome analysis revealed their potential role as (poly)saccharide degraders in freshwater, uncovered interesting genomic features for this lifestyle, and suggested their adaptation to nutrient availabilities in their environments.Verrucomicrobia populations differ significantly between the two lakes in glycoside hydrolase gene abundance and functional profiles, reflecting the autochthonous and terrestrially derived allochthonous carbon sources of the two ecosystems, respectively. Interestingly, a number of genomes recovered from the bog contained gene clusters that potentially encode a novel porin-multiheme cytochrome c complex and might be involved in extracellular electron transfer in the anoxic humus-rich environment. Notably, most epilimnion genomes have large numbers of so-called “Planctomycete-specific” cytochrome c-encoding genes, which exhibited distribution patterns nearly opposite to those seen with glycoside hydrolase genes, probably associated withmore » the different levels of environmental oxygen availability and carbohydrate complexity between lakes/layers. Overall, the recovered genomes represent a major step toward understanding the role, ecophysiology, and distribution of Verrucomicrobia in freshwater. Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. We greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling.« less

Authors:

He, Shaomei ^[1]; Stevens, Sarah L. R. ^[2]; Chan, Leong-Keat ^[3]; Bertilsson, Stefan ^[4]; Glavina del Rio, Tijana ^[3]; Tringe, Susannah G. ^[3]; Malmstrom, Rex R. ^[3]; McMahon, Katherine D.  ^[5];

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Hallam, ed., Steven J.

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+ Show Author Affiliations

1. Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA, Department of Geoscience, University of Wisconsin—Madison, Madison, Wisconsin, USA
2. Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
3. DOE Joint Genome Institute, Walnut Creek, California, USA
4. Department of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden
5. Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA, Department of Civil and Environmental Engineering, University of Wisconsin—Madison, Madison, Wisconsin, USA

Publication Date:

Wed Oct 25 00:00:00 EDT 2017

Research Org.:

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; USDA National Inst. of Food and Agriculture (NIFA); National Science Foundation (NSF)

OSTI Identifier:

1615077

Alternate Identifier(s):

OSTI ID: 1459395

Grant/Contract Number:  

AC02-05CH11231; MCB-0702395; NTL-LTER DEB-1440297; DEB-1344254; 1002996

Resource Type:

Published Article

Journal Name:

mSphere

Additional Journal Information:

Journal Name: mSphere Journal Volume: 2 Journal Issue: 5; Journal ID: ISSN 2379-5042

Publisher:

American Society for Microbiology

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES