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  • 1.
    Garcia, Sarahi L.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
    Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions2016In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 77, no 2, p. 79-85Article in journal (Refereed)
    Abstract [en]

    Even though thousands of microbial strains have now been successfully cultivated and described, these only represent a small fraction of global microbial diversity. Moreover, many of the ubiquitous and abundant environmental microorganisms still defy axenic cultivation. Here, I present mixed cultures as a powerful tool to cultivate and study ubiquitous but hard-to-cultivate microorganisms. A mixed culture is a subsample from a complex natural community that contains 2 or more microbial strains. When cultivated together with their metabolic partners, these ubiquitous microorganisms can mutually satisfy metabolic dependencies just as they do in the environment. By reducing the complexity while keeping some diversity, mixed cultures can then be used as model communities. Furthermore, by combining the relative simplicity of these model communities with molecular and bioinformatics tools, the complex natural interactions could be deciphered one model community at a time. Ultimately, mixed cultures can be used to generate a working hypothesis to explore the microbial ecology and genetic population structures of the unseen vast majority of microorganisms.

  • 2.
    Garcia, Sarahi L.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Buck, Moritz
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    McMahon, Katherine D.
    Univ Wisconsin, Dept Bacteriol, Madison, WI 53706 USA.;Univ Wisconsin, Dept Civil & Environm Engn, Madison, WI 53706 USA..
    Grossart, Hans-Peter
    Leibniz Inst Freshwater Ecol & Inland Fisheries, Dept Expt Limnol, D-16775 Ot Neuglobsow, Stechlin, Germany.;Univ Potsdam, Inst Biochem & Biol, D-14476 Potsdam, Germany..
    Eiler, Alexander
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Warnecke, Falk
    Univ Jena, Jena Sch Microbial Commun, D-07743 Jena, Germany..
    Auxotrophy and intrapopulation complementary in the "interactome' of a cultivated freshwater model community2015In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 24, no 17, p. 4449-4459Article in journal (Refereed)
    Abstract [en]

    Microorganisms are usually studied either in highly complex natural communities or in isolation as monoclonal model populations that we manage to grow in the laboratory. Here, we uncover the biology of some of the most common and yet-uncultured bacteria in freshwater environments using a mixed culture from Lake Grosse Fuchskuhle. From a single shotgun metagenome of a freshwater mixed culture of low complexity, we recovered four high-quality metagenome-assembled genomes (MAGs) for metabolic reconstruction. This analysis revealed the metabolic interconnectedness and niche partitioning of these naturally dominant bacteria. In particular, vitamin- and amino acid biosynthetic pathways were distributed unequally with a member of Crenarchaeota most likely being the sole producer of vitamin B12 in the mixed culture. Using coverage-based partitioning of the genes recovered from a single MAG intrapopulation metabolic complementarity was revealed pointing to social' interactions for the common good of populations dominating freshwater plankton. As such, our MAGs highlight the power of mixed cultures to extract naturally occurring interactomes' and to overcome our inability to isolate and grow the microbes dominating in nature.

  • 3.
    Garcia, Sarahi L
    et al.
    University of Georgia, Biorefining and Carbon Cycling Program, Department of Biological and Agricultural Engineering, Athens.
    Jangid, Kamlesh
    Whitman, William B
    Das, K C
    Transition of microbial communities during the adaption to anaerobic digestion of carrot waste2011In: Bioresource technology, Vol. 102, no 15, p. 7249-7256Article in journal (Refereed)
  • 4.
    Garcia, Sarahi L
    et al.
    ena School for Microbial Communication (JSMC) and Microbial Ecology Group at Friedrich Schiller University Jena, Germany..
    McMahon, Katherine D
    Grossart, Hans-Peter
    Warnecke, Falk
    Successful enrichment of the ubiquitous freshwater acI Actinobacteria2014In: Environmental Microbiology Reports, ISSN 1758-2229, E-ISSN 1758-2229, Vol. 6, no 1, p. 21-27Article in journal (Refereed)
    Abstract [en]

    Actinobacteriaof the acI lineage are often thenumerically dominant bacterial phylum in surfacefreshwaters, where they can account for>50% oftotal bacteria. Despite their abundance, there are nodescribed isolates. In an effort to obtain enrichmentof these ubiquitous freshwaterActinobacteria, dilutedfreshwater samples from Lake Grosse Fuchskuhle,Germany, were incubated in 96-well culture plates.With this method, a successful enrichment containinghigh abundances of a member of the lineage acI wasestablished. Phylogenetic classification showed thatthe acIActinobacteriaof the enrichment belonged tothe acI-B2 tribe, which seems to prefer acidic lakes.This enrichment grows to low cell densities and thusthe oligotrophic nature of acI-B2 was confirmed.

  • 5.
    Garcia, Sarahi L
    et al.
    Jena School for Microbial Communication (JSMC) and Microbial Ecology Group at Friedrich Schiller University Jena, Jena, Germany.
    McMahon, Katherine D
    Martinez-Garcia, Manuel
    Srivastava, Abhishek
    Sczyrba, Alexander
    Stepanauskas, Ramunas
    Grossart, Hans-Peter
    Woyke, Tanja
    Warnecke, Falk
    Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton2013In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 7, no 1, p. 137-147Article in journal (Refereed)
    Abstract [en]

    Actinobacteria within the acI lineage are often numerically dominating in freshwater ecosystems, where they can account for >50% of total bacteria in the surface water. However, they remain uncultured to date. We thus set out to use single-cell genomics to gain insights into their genetic make-up, with the aim of learning about their physiology and ecological niche. A representative from the highly abundant acI-B1 group was selected for shotgun genomic sequencing. We obtained a draft genomic sequence in 75 larger contigs (sum=1.16 Mb), with an unusually low genomic G+C mol% (~42%). Actinobacteria core gene analysis suggests an almost complete genome recovery. We found that the acI-B1 cell had a small genome, with a rather low percentage of genes having no predicted functions (~15%) as compared with other cultured and genome-sequenced microbial species. Our metabolic reconstruction hints at a facultative aerobe microorganism with many transporters and enzymes for pentoses utilization (for example, xylose). We also found an actinorhodopsin gene that may contribute to energy conservation under unfavorable conditions. This project reveals the metabolic potential of a member of the global abundant freshwater Actinobacteria.

  • 6.
    Garcia, Sarahi L
    et al.
    ena School for Microbial Communication (JSMC) and Microbial Ecology Group at Friedrich Schiller University Jena, Germany.
    Salka, Ivette
    Grossart, Hans-Peter
    Warnecke, Falk
    Depth-discrete profiles of bacterial communities reveal pronounced spatio-temporal dynamics related to lake stratification2013In: Environmental Microbiology Reports, ISSN 1758-2229, E-ISSN 1758-2229, Vol. 5, no 4, p. 549-555Article in journal (Refereed)
  • 7.
    Garcia, Sarahi L
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Uppsala University, Science for Life Laboratory, SciLifeLab. University of Wisconsin-Madison, Madison, USA.
    Stevens, Sarah L R
    University of Wisconsin-Madison, Madison, USA.
    Crary, Benjamin
    University of Wisconsin-Madison, Madison, USA.
    Martinez-Garcia, Manuel
    University of Alicante, Alicante, Spain.
    Stepanauskas, Ramunas
    Bigelow Laboratory for Ocean Sciences, East Boothbay, USA.
    Woyke, Tanja
    DOE Joint Genome Institute, Walnut Creek, USA.
    Tringe, Susannah G
    DOE Joint Genome Institute, Walnut Creek, USA.
    Andersson, Siv G E
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Bertilsson, Stefan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Malmstrom, Rex R
    DOE Joint Genome Institute, Walnut Creek, USA.
    McMahon, Katherine D
    University of Wisconsin-Madison, Madison, USA.
    Contrasting patterns of genome-level diversity across distinct co-occurring bacterial populations2018In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 12, no 3, p. 742-755Article in journal (Refereed)
    Abstract [en]

    To understand the forces driving differentiation and diversification in wild bacterial populations, we must be able to delineate and track ecologically relevant units through space and time. Mapping metagenomic sequences to reference genomes derived from the same environment can reveal genetic heterogeneity within populations, and in some cases, be used to identify boundaries between genetically similar, but ecologically distinct, populations. Here we examine population-level heterogeneity within abundant and ubiquitous freshwater bacterial groups such as the acI Actinobacteria and LD12 Alphaproteobacteria (the freshwater sister clade to the marine SAR11) using 33 single-cell genomes and a 5-year metagenomic time series. The single-cell genomes grouped into 15 monophyletic clusters (termed "tribes") that share at least 97.9% 16S rRNA identity. Distinct populations were identified within most tribes based on the patterns of metagenomic read recruitments to single-cell genomes representing these tribes. Genetically distinct populations within tribes of the acI Actinobacterial lineage living in the same lake had different seasonal abundance patterns, suggesting these populations were also ecologically distinct. In contrast, sympatric LD12 populations were less genetically differentiated. This suggests that within one lake, some freshwater lineages harbor genetically discrete (but still closely related) and ecologically distinct populations, while other lineages are composed of less differentiated populations with overlapping niches. Our results point at an interplay of evolutionary and ecological forces acting on these communities that can be observed in real time.

  • 8. Ghylin, Trevor W
    et al.
    Garcia, Sarahi L
    Moya, Francisco
    Oyserman, Ben O
    Schwientek, Patrick
    Forest, Katrina T
    Mutschler, James
    Dwulit-Smith, Jeffrey
    Chan, Leong-Keat
    Martinez-Garcia, Manuel
    Sczyrba, Alexander
    Stepanauskas, Ramunas
    Grossart, Hans-Peter
    Woyke, Tanja
    Warnecke, Falk
    Malmstrom, Rex
    Bertilsson, Stefan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
    McMahon, Katherine D
    Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage2014In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 8, no 12, p. 2503-2516Article in journal (Refereed)
    Abstract [en]

    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.

  • 9.
    Hamilton, Joshua J.
    et al.
    University of Wisconsin—Madison, Madison, USA.
    Garcia, Sarahi L.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
    Brown, Brittany S.
    University of Wisconsin—Madison, Madison, USA.
    Oyserman, Ben O.
    University of Wisconsin—Madison, Madison, USA.
    Moya-Flores, Francisco
    University of Wisconsin—Madison, Madison, USA.
    Bertilsson, Stefan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Malmstrom, Rex R.
    United States Department of Energy Joint Genome Institute, Walnut Creek, USA.
    Forest, Katrina T.
    University of Wisconsin—Madison, Madison, USA.
    McMahon, Katherine D.
    University of Wisconsin—Madison, Madison, USA.
    Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI2017In: mSystems, E-ISSN 2379-5077, Vol. 2, no 4, article id e00091-17Article in journal (Refereed)
    Abstract [en]

    An explosion in the number of available genome sequences obtained through metagenomics and single-cell genomics has enabled a new view of the diversity of microbial life, yet we know surprisingly little about how microbes interact with each other or their environment. In fact, the majority of microbial species remain uncultivated, while our perception of their ecological niches is based on reconstruction of their metabolic potential. In this work, we demonstrate how the “seed set framework,” which computes the set of compounds that an organism must acquire from its environment (E. Borenstein, M. Kupiec, M. W. Feldman, and E. Ruppin, Proc Natl Acad Sci U S A 105:14482–14487, 2008, https://doi.org/10.1073/pnas.0806162105 ), enables computational analysis of metabolic reconstructions while providing new insights into a microbe’s metabolic capabilities, such as nutrient use and auxotrophies. We apply this framework to members of the ubiquitous freshwater actinobacterial lineage acI, confirming and extending previous experimental and genomic observations implying that acI bacteria are heterotrophs reliant on peptides and saccharides. We also present the first metatranscriptomic study of the acI lineage, revealing high expression of transport proteins and the light-harvesting protein actinorhodopsin. Putative transport proteins complement predictions of nutrients and essential metabolites while providing additional support of the hypothesis that members of the acI are photoheterotrophs.

  • 10. Salka, Ivette
    et al.
    Wurzbacher, Christian
    Garcia, Sarahi L
    ena School for Microbial Communication (JSMC) and Microbial Ecology Group, Friedrich Schiller University Jena, Philosophenweg 12, 07743 Jena, Germany..
    Labrenz, Matthias
    Jürgens, Klaus
    Grossart, Hans-Peter
    Distribution of acI-Actinorhodopsin genes in Baltic Sea salinity gradients indicates adaptation of facultative freshwater photoheterotrophs to brackish waters2014In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 16, no 2, p. 586-597Article in journal (Refereed)
    Abstract [en]

    Knowledge onActinobacteriarhodopsin gene (actR)diversity and spatial distribution is scarce. The BalticSea is characterized by strong salinity gradientsleading to the coexistence of marine and freshwaterbacteria and hence is an ideal study area to elucidatethe dispersion and phylogenetic affiliation ofactRindependence on salinity. ActRDGGE fingerprints insummer 2008 revealed between 3 and 19 distinctbands within a salinity range of 2.4–27 PSU. Environ-mentalactRclone sequences were obtained from sta-tions distributed along the whole salinity gradient.Overall, 20 differentactRsequence groups (opera-tional taxonomic units) were found, with up to 11different ones per station. Phylogenetically, theactRsequences were predominantly (80%) affiliated with freshwater acI-Actinobacteriawhose 16S rRNA geneaccounted for 2–33% of total 16S rRNA genes in both the Bothnian Sea and central Baltic Sea. However, atsalinities above 14 PSU, acI-16S rRNA gene accounted for less than 1%. In contrast, the diversity of actRremained high. Changes in actRgene diversity were significantly correlated with salinity, oxygen, silica orabundance of Synechococcussp. Our results demonstrate a wide distribution of freshwater actRalong theBaltic Sea salinity gradient indicating that some fresh-water Actinobacteriamight have adapted to higher salinities.

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