Integrated genomics provides insights for the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter
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Abstract
Candidatus Accumulibacter plays a major role in enhanced biological phosphorus removal (EBPR), but the key genomic elements in metagenome assembled genomes enabling their phosphorus cycling ability remain unclear. Pangenome analyses were performed to systematically compare the genomic makeup of Ca. Accumulibacter and non- Ca . Accumulibacter members within the Rhodocyclaceae family. Metatranscriptomic analyses of an enrichment culture of Ca. Accumulibacter clade IIC strain SCUT-2 were performed to investigate gene transcription characteristics in a typical anaerobic-aerobic cycle. Two hundred ninety-eight core genes were shown to be obtained by Ca. Accumulibacter at their least common ancestor. One hundred twenty-four of them were acquired via horizontal gene transfer (HGT) based on best-match analysis against the NCBI database. Fourty-four laterally derived genes were actively transcribed in a typical EBPR cycle, including the polyphosphate kinase 2 (PPK2) gene. Genes in the phosphate regulon (Pho) were poorly transcribed. Via a systematical analysis of the occurrences of these genes in closely related Dechloromonas -polyphosphate accumulating organisms (PAOs) and Propionivibrio -non-PAOs, a Pho dysregulation hypothesis is proposed to explain the mechanism of EBPR. It states that the PhoU acquired by HGT fails in regulating the high-affinity phosphate transport (Pst) system. To avoid phosphate poisoning, the laterally acquired PPK2 is employed to condense excess phosphate into polyphosphate. Alternatively, genes encoding PhoU and PPK2 are obtained from different donor bacteria, leading to unmatched phosphate concentration thresholds for their activation/inactivation. PPK2 tends to reduce the intracellular phosphate to concentration levels perceived by PhoU as low-phosphate states. PhoU is not activated to turn off the Pst system, resulting in continuous phosphate uptake. In conclusion, based on integrated genomic analyses, the HGT of pho U and ppk 2 and the resultant Pho dysregulation may have triggered the development and evolution of the P cycling trait in Ca. Accumulibacter.
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In addition, Ca. Dechloromonas phosporitropha were lack of pst, phoU, phoB and phoR genes in the Pho regulon, which is consistent with our hypothesis that the Pho regulation may not work properly in PAOs.
Interesting that Dechloromonas is missing this
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their encoding proteins (i.e., PhoU, PhoU homologue and PPK2) may have incompatible phosphate activation/inactivation thresholds.
This is an interesting hypothesis - are you able to maybe follow up with structural analyses looking at the Alphafold predictions for these proteins and docking simulations? Or compare to PPK2 in other bacteria known to use PPK1 and PPK2 for polyphosphate accumulation (such as P. aeruginosa) and see if the model holds there as well perhaps?
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In addition, three distant phoU homologs (NOF05_17860, NOF05_09930, NOF05_09935) were found in Ca. Accumulibacter genomes which are also horizontally acquired core genes. Distant homologs are pairs of proteins which have similar structures and functions but low gene sequence similarity (Monzon et al., 2022). The homolog phoU
This is interesting, but a little confusing here. Is the main phoU copy near pit, or is one of the distant homologs near it? If not, where are the distant homologs and how were they confirmed to be structural homologs, or were they annotated that way by KEGG?
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including the acetate kinase gene. These 42 gene families may not play a key role in the evolution of non-PAO to PAO due to their different transcription behaviors in SCUT-2 and UW1.
Perhaps, I think there is also demonstrated difference in acetate uptake kinetic rates between the clades/species
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Figure 6.
Panel C of this figure is a little unintuitive since the columns are ordered by the clustering of gene expression patterns and not ordered by time point, whereas panel B is ordered by timepoint
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Cluster 2 showed a pattern of increased transcription throughout the anaerobic period, peaking after oxygen exposure. The phosphate transport system substrate binding protein (pstS, NOF05_04305) and the laterally derived polyphosphate kinase 2 gene (ppk2, NOF05_17285) showed Cluster 2 transcription pattern.
This is interesting, and maybe the opposite of what I would expect. Since P is released during the anaerobic period, and consumption of PHA in aerobic period used to form polyP, I would expect ppk2 and the transporter to be highest in the aerobic period. Although I think this could be related to our results here: https://www.nature.com/articles/s43705-022-00189-2 where we found differentiation of expression patterns in PstSABC either highest at the beginning or end of the aerobic period, so to be high at the beginning of the …
Cluster 2 showed a pattern of increased transcription throughout the anaerobic period, peaking after oxygen exposure. The phosphate transport system substrate binding protein (pstS, NOF05_04305) and the laterally derived polyphosphate kinase 2 gene (ppk2, NOF05_17285) showed Cluster 2 transcription pattern.
This is interesting, and maybe the opposite of what I would expect. Since P is released during the anaerobic period, and consumption of PHA in aerobic period used to form polyP, I would expect ppk2 and the transporter to be highest in the aerobic period. Although I think this could be related to our results here: https://www.nature.com/articles/s43705-022-00189-2 where we found differentiation of expression patterns in PstSABC either highest at the beginning or end of the aerobic period, so to be high at the beginning of the aerobic period would have to increase in the anaerobic period.
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A further analysis of another 21 available Propionivibrio genomes further confirmed that ppk2 and phoU are differential genes between Ca. Accumulibacter and Propionivibrio.
Ah I see you compared to other Propionivibrio genomes here
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The pan PAO genome was compared to the Ca. Propionivibrio aalborgensis (a closely related GAO, Albertsen et al., 2016) genome to identify differential genes (defined as core genes present in the pan PAO genome but absent in the Ca. Propionivibrio aalborgensis genome).
Is this the only closely related non-PAO that was compared to? I think this is a HQ genome but there could be problems with making PAO-specific inferences comparing to just one non-PAO?
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a Pho dysregulation hypothesis is proposed to explain the mechanism of EBPR. It states that the PhoU acquired by HGT fails in regulating the high-affinity phosphate transport (Pst) system. To avoid phosphate poisoning, the laterally acquired PPK2 is employed to condense excess phosphate into polyphosphate.
This is interesting! Excited to read more and dive into this hypothesis! My gut reaction is if you have looked at other model organisms for polyphosphate accumulation such as E. coli, Pseudomonas aeruginosa, and Neisseria gonorhhoeae to see if they fit this model? I could imagine P. aeruginosa might since PPK2 is known to enhance polyP formation in virulence and biofilm formation of this pathogen
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