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Comparative single-cell genomics reveals potential ecological niches for the freshwater acl Actinobacteria lineage

  • Members of the acI lineage of Actinobacteria are the most abundant microorganisms in most freshwater lakes; however, our understanding of the keys to their success and their role in carbon and nutrient cycling in freshwater systems has been hampered by the lack of pure cultures and genomes. We obtained draft genome assemblies from 11 single cells representing three acI tribes (acI-A1, acI-A7, acI-B1) from four temperate lakes in the United States and Europe. Comparative analysis of acI SAGs and other available freshwater bacterial genomes showed that acI has more gene content directed toward carbohydrate acquisition as compared to Polynucleobacter and LD12 Alphaproteobacteria, which seem to specialize more on carboxylic acids. The acI genomes contain actinorhodopsin as well as some genes involved in anaplerotic carbon fixation indicating the capacity to supplement their known heterotrophic lifestyle. Genome-level differences between the acI-A and acI-B clades suggest specialization at the clade level for carbon substrate acquisition.Members of the acI lineage of Actinobacteria are the most abundant microorganisms in most freshwater lakes; however, our understanding of the keys to their success and their role in carbon and nutrient cycling in freshwater systems has been hampered by the lack of pure cultures and genomes. We obtained draft genome assemblies from 11 single cells representing three acI tribes (acI-A1, acI-A7, acI-B1) from four temperate lakes in the United States and Europe. Comparative analysis of acI SAGs and other available freshwater bacterial genomes showed that acI has more gene content directed toward carbohydrate acquisition as compared to Polynucleobacter and LD12 Alphaproteobacteria, which seem to specialize more on carboxylic acids. The acI genomes contain actinorhodopsin as well as some genes involved in anaplerotic carbon fixation indicating the capacity to supplement their known heterotrophic lifestyle. Genome-level differences between the acI-A and acI-B clades suggest specialization at the clade level for carbon substrate acquisition. Overall, the acI genomes appear to be highly streamlined versions of Actinobacteria that include some genes allowing it to take advantage of sunlight and N-rich organic compounds such as polyamines, di-and oligopeptides, branched-chain amino acids and cyanophycin. This work significantly expands the known metabolic potential of the cosmopolitan freshwater acI lineage and its ecological and genetic traits.show moreshow less

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Author details:Trevor W. Ghylin, Sarahi L. Garcia, Francisco Moya, Ben O. Oyserman, Patrick Schwientek, Katrina T. Forest, James Mutschler, Jeffrey Dwulit-Smith, Leong-Keat Chan, Manuel Martinez-Garcia, Alexander Sczyrba, Ramunas Stepanauskas, Hans-Peter GrossartORCiDGND, Tanja Woyke, Falk Warnecke, Rex Malmstrom, Stefan Bertilsson, Katherine D. McMahon
DOI:https://doi.org/10.1038/ismej.2014.135
ISSN:1751-7362
ISSN:1751-7370
Pubmed ID:https://pubmed.ncbi.nlm.nih.gov/25093637
Title of parent work (English):The ISME journal : multidisciplinary journal of microbial ecology
Publisher:Nature Publ. Group
Place of publishing:London
Publication type:Article
Language:English
Year of first publication:2014
Publication year:2014
Release date:2017/03/27
Volume:8
Issue:12
Number of pages:14
First page:2503
Last Page:2516
Funding institution:Join Genome Institute; Biotechnology Training Program of the National Institutes of Health at the University of Wisconsin-Madison [5T32GM08349]; Office of Science of the U.S. Department of Energy [DE-AC02-05CH11231]; United States National Science Foundation Microbial Observatories program [MCB-0702395]; Long Term Ecological Research program [NTL-LTER DEB-0822700]; INSPIRE award [DEB-1344254]; Swedish Wenner-Gren Foundation; National Institute of Food and Agriculture, United States Department of Agriculture [WIS01516]; United States National Science Foundation [DEB-0841933, OCE-0821374, EF-0633142, MCB-0738232]; Swedish Research Council; German Science Foundation [DFG GR1540/17-1]; JSMC
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Geowissenschaften
Peer review:Referiert
Institution name at the time of the publication:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Erd- und Umweltwissenschaften
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