title: Ancestral genome reconstruction identifies the evolutionary basis for trait acquisition in polyphosphate accumulating bacteria.
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.
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Ben O
authors.identifier: 0000-0001-9052-2651
authors.initials: BO
authors.lastname: Oyserman
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Francisco
authors.initials: F
authors.lastname: Moya
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Christopher E
authors.initials: CE
authors.lastname: Lawson
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Antonio L
authors.initials: AL
authors.lastname: Garcia
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Mark
authors.initials: M
authors.lastname: Vogt
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Mitchell
authors.initials: M
authors.lastname: Heffernen
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Daniel R
authors.initials: DR
authors.lastname: Noguera
authors.affiliation: Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.|Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Katherine D
authors.initials: KD
authors.lastname: McMahon
mesh_terms: D001419:Bacteria / Q000145:classification / Q000235:genetics* / Q000302:isolation & purification / Q000378:metabolism*; D019149:Bioreactors / Q000382:microbiology; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D006003:Glycogen / Q000378:metabolism; D010758:Phosphorus / Q000378:metabolism; D010802:Phylogeny; D011122:Polyphosphates / Q000378:metabolism*
chemical_list: D011122:Polyphosphates; D010758:Phosphorus; D006003:Glycogen