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Hamilton, J. J., Garcia, S. L., Brown, B. S., Oyserman, B. O., Moya-Flores, F., Bertilsson, S., . . . McMahon, K. D. (2017). Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI. mSystems, 2(4), Article ID e00091-17.
Open this publication in new window or tab >>Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
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2017 (English)In: mSystems, E-ISSN 2379-5077, Vol. 2, no 4, article id e00091-17Article in journal (Refereed) Published
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.

Keyword
freshwater microbial ecology, metabolism, metagenomics, metatranscriptomics, physiology, systems biology
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-339041 (URN)10.1128/mSystems.00091-17 (DOI)
Available from: 2018-01-15 Created: 2018-01-15 Last updated: 2018-01-19Bibliographically approved
Garcia, S. L. (2016). Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions. Aquatic Microbial Ecology, 77(2), 79-85
Open this publication in new window or tab >>Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions
2016 (English)In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 77, no 2, p. 79-85Article in journal (Refereed) Published
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.

Keyword
Microbial ecology, Mixed cultures, Model communities, Cultivation, Interactions, Dependencies, Auxotrophy
National Category
Ecology Microbiology
Identifiers
urn:nbn:se:uu:diva-305955 (URN)10.3354/ame01789 (DOI)000384308000002 ()
Available from: 2016-11-01 Created: 2016-10-24 Last updated: 2017-11-29Bibliographically approved
Garcia, S. L., Buck, M., McMahon, K. D., Grossart, H.-P., Eiler, A. & Warnecke, F. (2015). Auxotrophy and intrapopulation complementary in the "interactome' of a cultivated freshwater model community. Molecular Ecology, 24(17), 4449-4459
Open this publication in new window or tab >>Auxotrophy and intrapopulation complementary in the "interactome' of a cultivated freshwater model community
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2015 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 24, no 17, p. 4449-4459Article in journal (Refereed) Published
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.

Keyword
community, cultures, interactions, metagenomics, populations
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-262971 (URN)10.1111/mec.13319 (DOI)000360445700009 ()26179741 (PubMedID)
Funder
Swedish Research Council, 2012-4592
Available from: 2015-09-23 Created: 2015-09-23 Last updated: 2017-12-01Bibliographically approved
Ghylin, T. W., Garcia, S. L., Moya, F., Oyserman, B. O., Schwientek, P., Forest, K. T., . . . McMahon, K. D. (2014). Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage. The ISME Journal, 8(12), 2503-2516
Open this publication in new window or tab >>Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage
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2014 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 8, no 12, p. 2503-2516Article in journal (Refereed) Published
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.

National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-238735 (URN)10.1038/ismej.2014.135 (DOI)000345498200015 ()25093637 (PubMedID)
Available from: 2014-12-16 Created: 2014-12-16 Last updated: 2017-12-05Bibliographically approved
Salka, I., Wurzbacher, C., Garcia, S. L., Labrenz, M., Jürgens, K. & Grossart, H.-P. (2014). Distribution of acI-Actinorhodopsin genes in Baltic Sea salinity gradients indicates adaptation of facultative freshwater photoheterotrophs to brackish waters. Environmental Microbiology, 16(2), 586-597
Open this publication in new window or tab >>Distribution of acI-Actinorhodopsin genes in Baltic Sea salinity gradients indicates adaptation of facultative freshwater photoheterotrophs to brackish waters
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2014 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 16, no 2, p. 586-597Article in journal (Refereed) Published
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.

National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-279795 (URN)10. 1111/1462-2920.12185 (DOI)
Available from: 2016-03-03 Created: 2016-03-03 Last updated: 2017-11-30Bibliographically approved
Garcia, S. L., McMahon, K. D., Grossart, H.-P. & Warnecke, F. (2014). Successful enrichment of the ubiquitous freshwater acI Actinobacteria. Environmental Microbiology Reports, 6(1), 21-27
Open this publication in new window or tab >>Successful enrichment of the ubiquitous freshwater acI Actinobacteria
2014 (English)In: Environmental Microbiology Reports, ISSN 1758-2229, E-ISSN 1758-2229, Vol. 6, no 1, p. 21-27Article in journal (Refereed) Published
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.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-279800 (URN)10. 1111/1758-2229.12104 (DOI)
Available from: 2016-03-03 Created: 2016-03-03 Last updated: 2017-11-30Bibliographically approved
Garcia, S. L., Salka, I., Grossart, H.-P. & Warnecke, F. (2013). Depth-discrete profiles of bacterial communities reveal pronounced spatio-temporal dynamics related to lake stratification. Environmental Microbiology Reports, 5(4), 549-555
Open this publication in new window or tab >>Depth-discrete profiles of bacterial communities reveal pronounced spatio-temporal dynamics related to lake stratification
2013 (English)In: Environmental Microbiology Reports, ISSN 1758-2229, E-ISSN 1758-2229, Vol. 5, no 4, p. 549-555Article in journal (Refereed) Published
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-279794 (URN)10. 1111/1758-2229.12044 (DOI)
Available from: 2016-03-03 Created: 2016-03-03 Last updated: 2017-11-30Bibliographically approved
Garcia, S. L., McMahon, K. D., Martinez-Garcia, M., Srivastava, A., Sczyrba, A., Stepanauskas, R., . . . Warnecke, F. (2013). Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton. The ISME Journal, 7(1), 137-147
Open this publication in new window or tab >>Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton
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2013 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 7, no 1, p. 137-147Article in journal (Refereed) Published
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.

National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-279793 (URN)10.1038/ismej.2012.86 (DOI)
Available from: 2016-03-03 Created: 2016-03-03 Last updated: 2017-11-30Bibliographically approved
Garcia, S. L., Jangid, K., Whitman, W. B. & Das, K. C. (2011). Transition of microbial communities during the adaption to anaerobic digestion of carrot waste. Bioresource technology, 102(15), 7249-7256
Open this publication in new window or tab >>Transition of microbial communities during the adaption to anaerobic digestion of carrot waste
2011 (English)In: Bioresource technology, Vol. 102, no 15, p. 7249-7256Article in journal (Refereed) Published
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-279792 (URN)
Available from: 2016-03-03 Created: 2016-03-03 Last updated: 2016-03-07Bibliographically approved
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-8622-0308

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