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

• Published in: The ISME Journal Vol. 10; no. 12; pp. 2931 - 2945
• Main Authors: Oyserman, Ben O, Moya, Francisco, Lawson, Christopher E, Garcia, Antonio L, Vogt, Mark, Heffernen, Mitchell, Noguera, Daniel R, McMahon, Katherine D
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.12.2016; Nature Publishing Group
• Subjects: 14/32; 38/77; 45/22; 631/181/735; 631/326/171; 631/443/319; Bacteria - classification; Bacteria - genetics; Bacteria - isolation & purification; Bacteria - metabolism; BASIC BIOLOGICAL SCIENCES; Biomedical and Life Sciences; Bioreactors - microbiology; Ecology; Environmental microbiology; Environmental sciences & ecology; Evolution, Molecular; Evolutionary Biology; Gene Transfer, Horizontal; Glycogen - metabolism; Ion transport; Life Sciences; Metabolism; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Molecular evolution; Original; original-article; Phosphorus - metabolism; Phylogeny; Polyhydroxyalkanoates; Polyphosphates - metabolism; Wastewater treatment
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/ismej.2016.67

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.