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Nature Methods (2017-11-01) 14: 1045-1054
, November 01, 2017
By
Woyke, Tanja
; Doud, Devin F R
; Schulz, Frederik 
This review outlines experimental considerations, advances and challenges in microbial single-cell genome sequencing and discusses the applications and scientific questions that this approach enabled.
By
Scheuner, Carmen; Tindall, Brian J; Lu, Megan; Nolan, Matt; Lapidus, Alla; Cheng, Jan-Fang; Goodwin, Lynne; Pitluck, Sam; Huntemann, Marcel; Liolios, Konstantinos; Pagani, Ioanna; Mavromatis, Konstantinos; Ivanova, Natalia; Pati, Amrita; Chen, Amy; Palaniappan, Krishna; Jeffries, Cynthia D; Hauser, Loren; Land, Miriam; Mwirichia, Romano; Rohde, Manfred; Abt, Birte; Detter, John C; Woyke, Tanja; Eisen, Jonathan A; Markowitz, Victor; Hugenholtz, Philip; Göker, Markus; Kyrpides, Nikos C; Klenk, Hans-Peter
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Planctomyces brasiliensis Schlesner 1990 belongs to the order Planctomycetales, which differs from other bacterial taxa by several distinctive features such as internal cell compartmentalization, multiplication by forming buds directly from the spherical, ovoid or pear-shaped mother cell and a cell wall consisting of a proteinaceous layer rather than a peptidoglycan layer. The first strains of P. brasiliensis, including the type strain IFAM 1448T, were isolated from a water sample of Lagoa Vermelha, a salt pit near Rio de Janeiro, Brasil. This is the second completed genome sequence of a type strain of the genus Planctomyces to be published and the sixth type strain genome sequence from the family Planctomycetaceae. The 6,006,602 bp long genome with its 4,811 protein-coding and 54 RNA genes is a part of the GenomicEncyclopedia ofBacteriaandArchaea project. Phylogenomic analyses indicate that the classification within the Planctomycetaceae is partially in conflict with its evolutionary history, as the positioning of Schlesneria renders the genus Planctomyces paraphyletic. A re-analysis of published fatty-acid measurements also does not support the current arrangement of the two genera. A quantitative comparison of phylogenetic and phenotypic aspects indicates that the three Planctomyces species with type strains available in public culture collections should be placed in separate genera. Thus the genera Gimesia, Planctopirus and Rubinisphaera are proposed to accommodate P. maris, P. limnophilus and P. brasiliensis, respectively. Pronounced differences between the reported G + C content of Gemmata obscuriglobus, Singulisphaera acidiphila and Zavarzinella formosa and G + C content calculated from their genome sequences call for emendation of their species descriptions. In addition to other features, the range of G + C values reported for the genera within the Planctomycetaceae indicates that the descriptions of the family and the order should be emended.
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By
Hedlund, Brian P.; Dodsworth, Jeremy A.; Murugapiran, Senthil K.; Rinke, Christian; Woyke, Tanja
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Despite >130 years of microbial cultivation studies, many microorganisms remain resistant to traditional cultivation approaches, including numerous candidate phyla of bacteria and archaea. Unraveling the mysteries of these candidate phyla is a grand challenge in microbiology and is especially important in habitats where they are abundant, including some extreme environments and low-energy ecosystems. Over the past decade, parallel advances in DNA amplification, DNA sequencing and computing have enabled rapid progress on this problem, particularly through metagenomics and single-cell genomics. Although each approach suffers limitations, metagenomics and single-cell genomics are particularly powerful when combined synergistically. Studies focused on extreme environments have revealed the first substantial genomic information for several candidate phyla, encompassing putative acidophiles (Parvarchaeota), halophiles (Nanohaloarchaeota), thermophiles (Acetothermia, Aigarchaeota, Atribacteria, Calescamantes, Korarchaeota, and Fervidibacteria), and piezophiles (Gracilibacteria). These data have enabled insights into the biology of these organisms, including catabolic and anabolic potential, molecular adaptations to life in extreme environments, unique genomic features such as stop codon reassignments, and predictions about cell ultrastructure. In addition, the rapid expansion of genomic coverage enabled by these studies continues to yield insights into the early diversification of microbial lineages and the relationships within and between the phyla of Bacteria and Archaea. In the next 5 years, the genomic foliage within the tree of life will continue to grow and the study of yet-uncultivated candidate phyla will firmly transition into the post-genomic era.
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The ISME Journal (2013-01-01) 7: 137-147
, January 01, 2013
By
Garcia, Sarahi L; McMahon, Katherine D; Martinez-Garcia, Manuel; Srivastava, Abhishek; Sczyrba, Alexander; Stepanauskas, Ramunas; Grossart, Hans-Peter; Woyke, Tanja; Warnecke, Falk
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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.
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By
Dmytrenko, Oleg; Russell, Shelbi L; Loo, Wesley T; Fontanez, Kristina M; Liao, Li; Roeselers, Guus; Sharma, Raghav; Stewart, Frank J; Newton, Irene LG; Woyke, Tanja; Wu, Dongying; Lang, Jenna Morgan; Eisen, Jonathan A; Cavanaugh, Colleen M
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Background
Symbioses between chemoautotrophic bacteria and marine invertebrates are rare examples of living systems that are virtually independent of photosynthetic primary production. These associations have evolved multiple times in marine habitats, such as deep-sea hydrothermal vents and reducing sediments, characterized by steep gradients of oxygen and reduced chemicals. Due to difficulties associated with maintaining these symbioses in the laboratory and culturing the symbiotic bacteria, studies of chemosynthetic symbioses rely heavily on culture independent methods. The symbiosis between the coastal bivalve, Solemya velum, and its intracellular symbiont is a model for chemosynthetic symbioses given its accessibility in intertidal environments and the ability to maintain it under laboratory conditions. To better understand this symbiosis, the genome of the S. velum endosymbiont was sequenced.
Results
Relative to the genomes of obligate symbiotic bacteria, which commonly undergo erosion and reduction, the S. velum symbiont genome was large (2.7 Mb), GC-rich (51%), and contained a large number (78) of mobile genetic elements. Comparative genomics identified sets of genes specific to the chemosynthetic lifestyle and necessary to sustain the symbiosis. In addition, a number of inferred metabolic pathways and cellular processes, including heterotrophy, branched electron transport, and motility, suggested that besides the ability to function as an endosymbiont, the bacterium may have the capacity to live outside the host.
Conclusions
The physiological dexterity indicated by the genome substantially improves our understanding of the genetic and metabolic capabilities of the S. velum symbiont and the breadth of niches the partners may inhabit during their lifecycle.
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By
Meier-Kolthoff, Jan P; Hahnke, Richard L; Petersen, Jörn; Scheuner, Carmen; Michael, Victoria; Fiebig, Anne; Rohde, Christine; Rohde, Manfred; Fartmann, Berthold; Goodwin, Lynne A; Chertkov, Olga; Reddy, TBK; Pati, Amrita; Ivanova, Natalia N; Markowitz, Victor; Kyrpides, Nikos C; Woyke, Tanja; Göker, Markus; Klenk, Hans-Peter
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Although Escherichia coli is the most widely studied bacterial model organism and often considered to be the model bacterium per se, its type strain was until now forgotten from microbial genomics. As a part of the GenomicEncyclopedia ofBacteria andArchaea project, we here describe the features of E. coli DSM 30083T together with its genome sequence and annotation as well as novel aspects of its phenotype. The 5,038,133 bp containing genome sequence includes 4,762 protein-coding genes and 175 RNA genes as well as a single plasmid. Affiliation of a set of 250 genome-sequenced E. coli strains, Shigella and outgroup strains to the type strain of E. coli was investigated using digital DNA:DNA-hybridization (dDDH) similarities and differences in genomic G+C content. As in the majority of previous studies, results show Shigella spp. embedded within E. coli and in most cases forming a single subgroup of it. Phylogenomic trees also recover the proposed E. coli phylotypes as monophyla with minor exceptions and place DSM 30083T in phylotype B2 with E. coli S88 as its closest neighbor. The widely used lab strain K-12 is not only genomically but also physiologically strongly different from the type strain. The phylotypes do not express a uniform level of character divergence as measured using dDDH, however, thus an alternative arrangement is proposed and discussed in the context of bacterial subspecies. Analyses of the genome sequences of a large number of E. coli strains and of strains from > 100 other bacterial genera indicate a value of 79-80% dDDH as the most promising threshold for delineating subspecies, which in turn suggests the presence of five subspecies within E. coli.
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By
Klonowska, Agnieszka; Moulin, Lionel; Ardley, Julie Kaye; Braun, Florence; Gollagher, Margaret Mary; Zandberg, Jaco Daniel; Marinova, Dora Vasileva; Huntemann, Marcel; Reddy, T. B. K.; Varghese, Neha Jacob; Woyke, Tanja; Ivanova, Natalia; Seshadri, Rekha; Kyrpides, Nikos; Reeve, Wayne Gerald
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Background
Cupriavidus strain STM 6070 was isolated from nickel-rich soil collected near Koniambo massif, New Caledonia, using the invasive legume trap host Mimosa pudica. STM 6070 is a heavy metal-tolerant strain that is highly effective at fixing nitrogen with M. pudica. Here we have provided an updated taxonomy for STM 6070 and described salient features of the annotated genome, focusing on heavy metal resistance (HMR) loci and heavy metal efflux (HME) systems.
Results
The 6,771,773 bp high-quality-draft genome consists of 107 scaffolds containing 6118 protein-coding genes. ANI values show that STM 6070 is a new species of Cupriavidus. The STM 6070 symbiotic region was syntenic with that of the M. pudica-nodulating Cupriavidus taiwanensis LMG 19424T. In contrast to the nickel and zinc sensitivity of C. taiwanensis strains, STM 6070 grew at high Ni2+ and Zn2+ concentrations. The STM 6070 genome contains 55 genes, located in 12 clusters, that encode HMR structural proteins belonging to the RND, MFS, CHR, ARC3, CDF and P-ATPase protein superfamilies. These HMR molecular determinants are putatively involved in arsenic (ars), chromium (chr), cobalt-zinc-cadmium (czc), copper (cop, cup), nickel (nie and nre), and silver and/or copper (sil) resistance. Seven of these HMR clusters were common to symbiotic and non-symbiotic Cupriavidus species, while four clusters were specific to STM 6070, with three of these being associated with insertion sequences. Within the specific STM 6070 HMR clusters, three novel HME-RND systems (nieIC cep nieBA, czcC2B2A2, and hmxB zneAC zneR hmxS) were identified, which constitute new candidate genes for nickel and zinc resistance.
Conclusions
STM 6070 belongs to a new Cupriavidus species, for which we have proposed the name Cupriavidus neocaledonicus sp. nov.. STM6070 harbours a pSym with a high degree of gene conservation to the pSyms of M. pudica-nodulating C. taiwanensis strains, probably as a result of recent horizontal transfer. The presence of specific HMR clusters, associated with transposase genes, suggests that the selection pressure of the New Caledonian ultramafic soils has driven the specific adaptation of STM 6070 to heavy-metal-rich soils via horizontal gene transfer.
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By
Jarett, Jessica K.
; Nayfach, Stephen; Podar, Mircea; Inskeep, William; Ivanova, Natalia N.; Munson-McGee, Jacob; Schulz, Frederik; Young, Mark; Jay, Zackary J.; Beam, Jacob P.; Kyrpides, Nikos C.; Malmstrom, Rex R.
; Stepanauskas, Ramunas; Woyke, Tanja
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Background
Nanoarchaeota are obligate symbionts of other Archaea first discovered 16 years ago, yet little is known about this largely uncultivated taxon. While Nanoarchaeota diversity has been detected in a variety of habitats using 16S rRNA gene surveys, genome sequences have been available for only three Nanoarchaeota and their hosts. The host range and adaptation of Nanoarchaeota to a wide range of environmental conditions has thus largely remained elusive. Single-cell genomics is an ideal approach to address these questions as Nanoarchaeota can be isolated while still attached to putative hosts, enabling the exploration of cell-cell interactions and fine-scale genomic diversity.
Results
From 22 single amplified genomes (SAGs) from three hot springs in Yellowstone National Park, we derived a genome-based phylogeny of the phylum Nanoarchaeota, linking it to global 16S rRNA gene diversity. By exploiting sequencing of co-sorted tightly attached cells, we associated Nanoarchaeota with 6 novel putative hosts, 2 of which were found in multiple SAGs, and showed that the same host species may associate with multiple species of Nanoarchaeota. Comparison of single nucleotide polymorphisms (SNPs) within a population of Nanoarchaeota SAGs indicated that Nanoarchaeota attached to a single host cell in situ are likely clonal. In addition to an overall pattern of purifying selection, we found significantly higher densities of non-synonymous SNPs in hypothetical cell surface proteins, as compared to other functional categories. Genes implicated in interactions in other obligate microbe-microbe symbioses, including those encoding a cytochrome bd-I ubiquinol oxidase and a FlaJ/TadC homologue possibly involved in type IV pili production, also had relatively high densities of non-synonymous SNPs.
Conclusions
This population genetics study of Nanoarchaeota greatly expands the known potential host range of the phylum and hints at what genes may be involved in adaptation to diverse environments or different hosts. We provide the first evidence that Nanoarchaeota cells attached to the same host cell are clonal and propose a hypothesis for how clonality may occur despite diverse symbiont populations.
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By
Hug, Laura A; Castelle, Cindy J; Wrighton, Kelly C; Thomas, Brian C; Sharon, Itai; Frischkorn, Kyle R; Williams, Kenneth H; Tringe, Susannah G; Banfield, Jillian F
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Background
Sediments are massive reservoirs of carbon compounds and host a large fraction of microbial life. Microorganisms within terrestrial aquifer sediments control buried organic carbon turnover, degrade organic contaminants, and impact drinking water quality. Recent 16S rRNA gene profiling indicates that members of the bacterial phylum Chloroflexi are common in sediment. Only the role of the class Dehalococcoidia, which degrade halogenated solvents, is well understood. Genomic sampling is available for only six of the approximate 30 Chloroflexi classes, so little is known about the phylogenetic distribution of reductive dehalogenation or about the broader metabolic characteristics of Chloroflexi in sediment.
Results
We used metagenomics to directly evaluate the metabolic potential and diversity of Chloroflexi in aquifer sediments. We sampled genomic sequence from 86 Chloroflexi representing 15 distinct lineages, including members of eight classes previously characterized only by 16S rRNA sequences. Unlike in the Dehalococcoidia, genes for organohalide respiration are rare within the Chloroflexi genomes sampled here. Near-complete genomes were reconstructed for three Chloroflexi. One, a member of an unsequenced lineage in the Anaerolinea, is an aerobe with the potential for respiring diverse carbon compounds. The others represent two genomically unsampled classes sibling to the Dehalococcoidia, and are anaerobes likely involved in sugar and plant-derived-compound degradation to acetate. Both fix CO2 via the Wood-Ljungdahl pathway, a pathway not previously documented in Chloroflexi. The genomes each encode unique traits apparently acquired from Archaea, including mechanisms of motility and ATP synthesis.
Conclusions
Chloroflexi in the aquifer sediments are abundant and highly diverse. Genomic analyses provide new evolutionary boundaries for obligate organohalide respiration. We expand the potential roles of Chloroflexi in sediment carbon cycling beyond organohalide respiration to include respiration of sugars, fermentation, CO2 fixation, and acetogenesis with ATP formation by substrate-level phosphorylation.
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By
Mukherjee, Supratim; Lapidus, Alla; Shapiro, Nicole; Cheng, Jan-Fang; Han, James; Reddy, TBK; Huntemann, Marcel; Ivanova, Natalia; Mikhailova, Natalia; Chen, Amy; Palaniappan, Krishna; Spring, Stefan; Göker, Markus; Markowitz, Victor; Woyke, Tanja; Tindall, Brian J; Klenk, Hans-Peter; Kyrpides, Nikos C; Pati, Amrita
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Pontibacter roseus is a member of genus Pontibacter family Cytophagaceae, class Cytophagia. While the type species of the genus Pontibacter actiniarum was isolated in 2005 from a marine environment, subsequent species of the same genus have been found in different types of habitats ranging from seawater, sediment, desert soil, rhizosphere, contaminated sites, solar saltern and muddy water. Here we describe the features of Pontibacter roseus strain SRC-1T along with its complete genome sequence and annotation from a culture of DSM 17521T. The 4,581,480 bp long draft genome consists of 12 scaffolds with 4,003 protein-coding and 50 RNA genes and is a part of Genomic Encyclopedia of Type Strains: KMG-I project.
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