Hugenholtz Philip

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Hugenholtz
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Philip
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  • Article
    Insights into the phylogeny and coding potential of microbial dark matter
    (Nature Publishing Group, 2013-07-14) Rinke, Christian ; Schwientek, Patrick ; Sczyrba, Alexander ; Ivanova, Natalia N. ; Anderson, Iain J. ; Cheng, Jan-Fang ; Darling, Aaron ; Malfatti, Stephanie A. ; Swan, Brandon K. ; Gies, Esther A. ; Dodsworth, Jeremy A. ; Hedlund, Brian P. ; Tsiamis, Georgios ; Sievert, Stefan M. ; Liu, Wen-Tso ; Eisen, Jonathan A. ; Hallam, Steven J. ; Kyrpides, Nikos C. ; Stepanauskas, Ramunas ; Rubin, Edward M. ; Hugenholtz, Philip ; Woyke, Tanja
    Genome sequencing enhances our understanding of the biological world by providing blueprints for the evolutionary and functional diversity that shapes the biosphere. However, microbial genomes that are currently available are of limited phylogenetic breadth, owing to our historical inability to cultivate most microorganisms in the laboratory. We apply single-cell genomics to target and sequence 201 uncultivated archaeal and bacterial cells from nine diverse habitats belonging to 29 major mostly uncharted branches of the tree of life, so-called ‘microbial dark matter’. With this additional genomic information, we are able to resolve many intra- and inter-phylum-level relationships and to propose two new superphyla. We uncover unexpected metabolic features that extend our understanding of biology and challenge established boundaries between the three domains of life. These include a novel amino acid use for the opal stop codon, an archaeal-type purine synthesis in Bacteria and complete sigma factors in Archaea similar to those in Bacteria. The single-cell genomes also served to phylogenetically anchor up to 20% of metagenomic reads in some habitats, facilitating organism-level interpretation of ecosystem function. This study greatly expands the genomic representation of the tree of life and provides a systematic step towards a better understanding of biological evolution on our planet.
  • Article
    Addendum: Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.)
    (Frontiers Media, 2018-04-18) Waite, David W. ; Vanwonterghem, Inka ; Rinke, Christian ; Parks, Donovan H. ; Zhang, Ying ; Takai, Ken ; Sievert, Stefan M. ; Simon, Jörg ; Campbell, Barbara J. ; Hanson, Thomas E. ; Woyke, Tanja ; Klotz, Martin G. ; Hugenholtz, Philip
  • Preprint
    Minimum information about a marker gene sequence (MIMARKS) and minimum information about any (x) sequence (MIxS) specifications
    ( 2011-01-04) Yilmaz, Pelin ; Kottmann, Renzo ; Field, Dawn ; Knight, Rob ; Cole, James R. ; Amaral-Zettler, Linda A. ; Gilbert, Jack A. ; Karsch-Mizrachi, Ilene ; Johnston, Anjanette ; Cochrane, Guy R. ; Vaughan, Robert ; Hunter, Christopher ; Park, Joonhong ; Morrison, Norman ; Rocca-Serra, Philippe ; Sterk, Peter ; Arumugam, Manimozhiyan ; Bailey, Mark ; Baumgartner, Laura ; Birren, Bruce W. ; Blaser, Martin J. ; Bonazzi, Vivien ; Booth, Tim ; Bork, Peer ; Bushman, Frederic D. ; Buttigieg, Pier Luigi ; Chain, Patrick S. G. ; Charlson, Emily ; Costello, Elizabeth K. ; Huot-Creasy, Heather ; Dawyndt, Peter ; DeSantis, Todd ; Fierer, Noah ; Fuhrman, Jed A. ; Gallery, Rachel E. ; Gevers, Dirk ; Gibbs, Richard A. ; San Gil, Inigo ; Gonzalez, Antonio ; Gordon, Jeffrey I. ; Guralnick, Robert P. ; Hankeln, Wolfgang ; Highlander, Sarah ; Hugenholtz, Philip ; Jansson, Janet K. ; Kau, Andrew L. ; Kelley, Scott T. ; Kennedy, Jerry ; Knights, Dan ; Koren, Omry ; Kuczynski, Justin ; Kyrpides, Nikos C. ; Larsen, Robert ; Lauber, Christian L. ; Legg, Teresa ; Ley, Ruth E. ; Lozupone, Catherine A. ; Ludwig, Wolfgang ; Lyons, Donna ; Maguire, Eamonn ; Methe, Barbara A. ; Meyer, Folker ; Muegge, Brian ; Nakielny, Sara ; Nelson, Karen E. ; Nemergut, Diana ; Neufeld, Josh D. ; Newbold, Lindsay K. ; Oliver, Anna E. ; Pace, Norman R. ; Palanisamy, Giriprakash ; Peplies, Jorg ; Petrosino, Joseph ; Proctor, Lita ; Pruesse, Elmar ; Quast, Christian ; Raes, Jeroen ; Ratnasingham, Sujeevan ; Ravel, Jacques ; Relman, David A. ; Assunta-Sansone, Susanna ; Schloss, Patrick D. ; Schriml, Lynn M. ; Sinha, Rohini ; Smith, Michelle I. ; Sodergren, Erica ; Spor, Ayme ; Stombaugh, Jesse ; Tiedje, James M. ; Ward, Doyle V. ; Weinstock, George M. ; Wendel, Doug ; White, Owen ; Whiteley, Andrew ; Wilke, Andreas ; Wortman, Jennifer R. ; Yatsunenko, Tanya ; Glockner, Frank Oliver
    Here we present a standard developed by the Genomic Standards Consortium (GSC) to describe marker gene sequences—the minimum information about a marker gene sequence (MIMARKS). We also introduce a system for describing the environment from which a biological sample originates. The “environmental packages” apply to any sequence whose origin is known and can therefore be used in combination with MIMARKS or other GSC checklists. Finally, to establish a unified standard for describing sequence data and to provide a single point of entry for the scientific community to access and learn about GSC checklists, we establish the minimum information about any (x) sequence (MIxS). Adoption of MIxS will enhance our ability to analyze natural genetic diversity across the Tree of Life as it is currently being documented by massive DNA sequencing efforts from myriad ecosystems in our ever-changing biosphere.
  • Article
    Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.)
    (Frontiers Media, 2017-04-24) Waite, David W. ; Vanwonterghem, Inka ; Rinke, Christian ; Parks, Donovan H. ; Zhang, Ying ; Takai, Ken ; Sievert, Stefan M. ; Simon, Jörg ; Campbell, Barbara J. ; Hanson, Thomas E. ; Woyke, Tanja ; Klotz, Martin G. ; Hugenholtz, Philip
    The Epsilonproteobacteria is the fifth validly described class of the phylum Proteobacteria, known primarily for clinical relevance and for chemolithotrophy in various terrestrial and marine environments, including deep-sea hydrothermal vents. As 16S rRNA gene repositories have expanded and protein marker analysis become more common, the phylogenetic placement of this class has become less certain. A number of recent analyses of the bacterial tree of life using both 16S rRNA and concatenated marker gene analyses have failed to recover the Epsilonproteobacteria as monophyletic with all other classes of Proteobacteria. In order to address this issue, we investigated the phylogenetic placement of this class in the bacterial domain using 16S and 23S rRNA genes, as well as 120 single-copy marker proteins. Single- and concatenated-marker trees were created using a data set of 4,170 bacterial representatives, including 98 Epsilonproteobacteria. Phylogenies were inferred under a variety of tree building methods, with sequential jackknifing of outgroup phyla to ensure robustness of phylogenetic affiliations under differing combinations of bacterial genomes. Based on the assessment of nearly 300 phylogenetic tree topologies, we conclude that the continued inclusion of Epsilonproteobacteria within the Proteobacteria is not warranted, and that this group should be reassigned to a novel phylum for which we propose the name Epsilonbacteraeota (phyl. nov.). We further recommend the reclassification of the order Desulfurellales (Deltaproteobacteria) to a novel class within this phylum and a number of subordinate changes to ensure consistency with the genome-based phylogeny. Phylogenomic analysis of 658 genomes belonging to the newly proposed Epsilonbacteraeota suggests that the ancestor of this phylum was an autotrophic, motile, thermophilic chemolithotroph that likely assimilated nitrogen from ammonium taken up from the environment or generated from environmental nitrate and nitrite by employing a variety of functional redox modules. The emergence of chemoorganoheterotrophic lifestyles in several Epsilonbacteraeota families is the result of multiple independent losses of various ancestral chemolithoautotrophic pathways. Our proposed reclassification of this group resolves an important anomaly in bacterial systematics and ensures that the taxonomy of Proteobacteria remains robust, specifically as genome-based taxonomies become more common.
  • Article
    Network-guided genomic and metagenomic analysis of the faecal microbiota of the critically endangered kakapo
    (Nature Publishing Group, 2018-05-25) Waite, David W. ; Dsouza, Melissa ; Sekiguchi, Yuji ; Hugenholtz, Philip ; Taylor, Michael W.
    The kakapo is a critically endangered, herbivorous parrot endemic to New Zealand. The kakapo hindgut hosts a dense microbial community of low taxonomic diversity, typically dominated by Escherichia fergusonii, and has proven to be a remarkably stable ecosystem, displaying little variation in core membership over years of study. To elucidate mechanisms underlying this robustness, we performed 16S rRNA gene-based co-occurrence network analysis to identify potential interactions between E. fergusonii and the wider bacterial community. Genomic and metagenomic sequencing were employed to facilitate interpretation of potential interactions observed in the network. E. fergusonii maintained very few correlations with other members of the microbiota, and isolates possessed genes for the generation of energy from a wide range of carbohydrate sources, including plant fibres such as cellulose. We surmise that this dominant microorganism is abundant not due to ecological interaction with other members of the microbiota, but its ability to metabolise a wide range of nutrients in the gut. This research represents the first concerted effort to understand the functional roles of the kakapo microbiota, and leverages metagenomic data to contextualise co-occurrence patterns. By combining these two techniques we provide a means for studying the diversity-stability hypothesis in the context of bacterial ecosystems.