Journal of Molecular Evolution

, Volume 86, Issue 7, pp 470–483 | Cite as

Investigation on the Evolutionary Relation of Diverse Polyhydroxyalkanoate Gene Clusters in Betaproteobacteria

  • Gurusamy Kutralam-Muniasamy
  • Rodolfo Marsch
  • Fermín Pérez-GuevaraEmail author
Original Article


Products of numerous genes (phaC, phaA, phaB, phaP, phaR, and phaZ) are involved in the synthesis and degradation processes of the ubiquitous prokaryotic polyhydroxyalkanoate (PHA) intracellular reserve storage system. In this study, we performed a bioinformatics analysis to identify PHA-related genes and proteins in the genome of 66 selected organisms (class: Betaproteobacteria) that occur in various habitats; besides, evolutionary trajectories of the PHA system are reported here. The identified PHA-related genes were organized into clusters, and the gene arrangement was highly diverse. The occurrence and distribution of PHA-related clusters revealed that a single cluster was primarily segmented into small gene groups among various genomes, which were further reorganized as novel clusters based on various functional genes. The individual phylogenies of gene and protein sequences supported that the clusters were assembled through the relocation of native orthologous genes that underwent insertion, deletion, and elongation events. Furthermore, the neighboring genes provided valuable evolutionary and functional cues regarding the conservation and maintenance of PHA-related genes in the genome. Overall, the aforementioned results strongly indicate the influence of horizontal gene transfer on the organization of PHA-related gene clusters. Therefore, our results reveal new insights into the organization, evolutionary history, and cluster conservation of the PHA-related gene inventories among Betaproteobacterial organisms.


Burkholderiaceae Cupriavidus necator H16 Phylogeny Flanking gene Gene relocation Horizontal gene transfer 



The authors express gratitude to Consejo Nacional de Ciencia y Tecnología (CB-2014-01; 236285 and Fronteras de la Ciencia 2015-1: 016) for financial support. The authors thank Miguel Angel Martínez Roque (UPIBI-IPN) for his assistance with data collection and artwork of this study. We are very grateful to Joel Alba Flores (Biotechnology and Bioengineering, CINVESTAV) and Ravi-Kumar Narayanasamy (Central University of Tamil Nadu) for fruitful discussions and valuable suggestions. We thank the editor and anonymous reviewer for their insightful comments, which helped us to improve the manuscript.

Supplementary material

239_2018_9859_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 14 KB)
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Table S2 Habitat characteristics of the representative Betaproteobacterial organisms (n = 66) (JPG 6142 KB)
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Fig. S1 Bayesian phylogeny of PhaB protein homologs of Rhodocyclaceae. Numbers at the nodes denote posterior probabilities (JPG 978 KB)
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Fig. S2 Phylogeny of phaB indicates multiple independent duplication events throughout its evolutionary history. (D: Duplication events). The reconciled phaB phylogenetic tree was obtained by means of NOTUNG v.2.9. It depicts 22 independent gene duplication events. All the duplication events appear toward the terminal nodes of the phylogenetic tree, indicating that these are recent events. Note: The homology analysis between phaB copies [phaB(1) and phaB(2)] revealed that they are merely <60% identical to each other. The results of the phylogeny analysis uncovered duplications (Fig. 2). Of note, gene duplications in the phaB gene family were found to initiate at the primary nodes of the reconciled phylogeny tree (Online Resource Fig. S2). According to these observations and wide variation in the sequence homology between the phaB copies, it is impossible to formulate a hypothesis regarding the duplication and speciation events after the emergence of Betaproteobacteria. Therefore, our interpretation is that the duplication and speciation occurred prior to the emergence of Betaproteobacteria. This assumption is supported by the orthologous relation of phaB genes as depicted in Fig. 2 and Online Resource Fig. S1. Nevertheless, the probable variations in the clade separation suggest that phaB1 instead of phaB2 might have been incorporated into the cluster during the evolutionary period of Betaproteobacteria. In-depth research is necessary to document the functional divergence (in terms of substrate specificity and enzymatic activity) of PhaB proteins in Betaproteobacteria (JPG 2.17 MB)
239_2018_9859_MOESM5_ESM.jpg (2.5 mb)
Fig. S3 Bayesian phylogeny trees of (a) PhaC, (b) PhaA, and (c) PhaR proteins. Numbers at the nodes indicate posterior probabilities (JPG 2.49 MB)
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Fig. S4 Phylogenetic incongruence of (a) phaC and 16S rRNA gene sequences (JPG 3.50 MB)
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Fig. S4 Phylogenetic incongruence of (b) of phaA and 16S rRNA gene sequences (JPG 3.37 MB)
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Fig. S4 Phylogenetic incongruence of (c) of phaR and 16S rRNA gene sequences (JPG 3.46 MB)


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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Gurusamy Kutralam-Muniasamy
    • 1
  • Rodolfo Marsch
    • 1
  • Fermín Pérez-Guevara
    • 1
    • 2
    Email author
  1. 1.Department of Biotechnology and BioengineeringCentro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexicoMexico
  2. 2.Nanoscience & Nanotechnology ProgramCentro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexicoMexico

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