Ancestral genome reconstruction identifies the evolutionary basis for trait acquisition in polyphosphate accumulating bacteria View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2016-04-29

AUTHORS

Ben O Oyserman, Francisco Moya, Christopher E Lawson, Antonio L Garcia, Mark Vogt, Mitchell Heffernen, Daniel R Noguera, Katherine D McMahon

ABSTRACT

The evolution of complex traits is hypothesized to occur incrementally. Identifying the transitions that lead to extant complex traits may provide a better understanding of the genetic nature of the observed phenotype. A keystone functional group in wastewater treatment processes are polyphosphate accumulating organisms (PAOs), however the evolution of the PAO phenotype has yet to be explicitly investigated and the specific metabolic traits that discriminate non-PAO from PAO are currently unknown. Here we perform the first comprehensive investigation on the evolution of the PAO phenotype using the model uncultured organism Candidatus Accumulibacter phosphatis (Accumulibacter) through ancestral genome reconstruction, identification of horizontal gene transfer, and a kinetic/stoichiometric characterization of Accumulibacter Clade IIA. The analysis of Accumulibacter’s last common ancestor identified 135 laterally derived genes, including genes involved in glycogen, polyhydroxyalkanoate, pyruvate and NADH/NADPH metabolisms, as well as inorganic ion transport and regulatory mechanisms. In contrast, pathways such as the TCA cycle and polyphosphate metabolism displayed minimal horizontal gene transfer. We show that the transition from non-PAO to PAO coincided with horizontal gene transfer within Accumulibacter’s core metabolism; likely alleviating key kinetic and stoichiometric bottlenecks, such as anaerobically linking glycogen degradation to polyhydroxyalkanoate synthesis. These results demonstrate the utility of investigating the derived genome of a lineage to identify key transitions leading to an extant complex phenotype. More... »

PAGES

2931-2945

References to SciGraph publications

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  • 2015-06-02. Tritagonist as a new term for uncharacterised microorganisms in environmental systems in THE ISME JOURNAL: MULTIDISCIPLINARY JOURNAL OF MICROBIAL ECOLOGY
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  • 2014-08-05. Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage in THE ISME JOURNAL: MULTIDISCIPLINARY JOURNAL OF MICROBIAL ECOLOGY
  • 2006-09-24. Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities in NATURE BIOTECHNOLOGY
  • Identifiers

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    http://scigraph.springernature.com/pub.10.1038/ismej.2016.67

    DOI

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    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/27128993


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    31 schema:description The evolution of complex traits is hypothesized to occur incrementally. Identifying the transitions that lead to extant complex traits may provide a better understanding of the genetic nature of the observed phenotype. A keystone functional group in wastewater treatment processes are polyphosphate accumulating organisms (PAOs), however the evolution of the PAO phenotype has yet to be explicitly investigated and the specific metabolic traits that discriminate non-PAO from PAO are currently unknown. Here we perform the first comprehensive investigation on the evolution of the PAO phenotype using the model uncultured organism Candidatus Accumulibacter phosphatis (Accumulibacter) through ancestral genome reconstruction, identification of horizontal gene transfer, and a kinetic/stoichiometric characterization of Accumulibacter Clade IIA. The analysis of Accumulibacter’s last common ancestor identified 135 laterally derived genes, including genes involved in glycogen, polyhydroxyalkanoate, pyruvate and NADH/NADPH metabolisms, as well as inorganic ion transport and regulatory mechanisms. In contrast, pathways such as the TCA cycle and polyphosphate metabolism displayed minimal horizontal gene transfer. We show that the transition from non-PAO to PAO coincided with horizontal gene transfer within Accumulibacter’s core metabolism; likely alleviating key kinetic and stoichiometric bottlenecks, such as anaerobically linking glycogen degradation to polyhydroxyalkanoate synthesis. These results demonstrate the utility of investigating the derived genome of a lineage to identify key transitions leading to an extant complex phenotype.
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    39 Candidatus Accumulibacter phosphatis
    40 IIA
    41 NADPH metabolism
    42 PaO
    43 TCA cycle
    44 acquisition
    45 analysis
    46 ancestor
    47 ancestral genome reconstruction
    48 bacteria
    49 basis
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    51 bottleneck
    52 characterization
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    55 complex phenotypes
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    57 comprehensive investigation
    58 contrast
    59 core metabolism
    60 cycle
    61 degradation
    62 evolution
    63 evolutionary basis
    64 first comprehensive investigation
    65 functional groups
    66 gene transfer
    67 genes
    68 genetic nature
    69 genome
    70 genome reconstruction
    71 glycogen
    72 glycogen degradation
    73 group
    74 horizontal gene transfer
    75 identification
    76 inorganic ion transport
    77 investigation
    78 ion transport
    79 key transitions
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    81 last common ancestor
    82 lineages
    83 mechanism
    84 metabolic traits
    85 metabolism
    86 nature
    87 observed phenotype
    88 organisms
    89 pathway
    90 phenotype
    91 polyphosphate
    92 polyphosphate metabolism
    93 process
    94 reconstruction
    95 regulatory mechanisms
    96 results
    97 specific metabolic traits
    98 stoichiometric characterization
    99 synthesis
    100 trait acquisition
    101 traits
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    109 schema:name Ancestral genome reconstruction identifies the evolutionary basis for trait acquisition in polyphosphate accumulating bacteria
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