Phylogenetic diversification and developmental implications of poly-(R)-3-hydroxyalkanoate gene cluster assembly in prokaryotes

Kutralam-Muniasamy, Gurusamy; Corona-Hernández, Juan; Narayanasamy, Ravi-Kumar; Marsch, Rodolfo; Pérez-Guevara, Fermín

doi:10.1093/femsle/fnx135

Cited by 11 publications

(5 citation statements)

References 36 publications

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“…In Halomonas sp. 363, the PHA genes were scattered around the genome, as has been observed in other Halomonas strains ( 34 – 36 ), whereas in Paracoccus sp. 392 two gene clusters ( phaRPCZ and phaAB ) were identified ( Fig.…”

Section: Resultssupporting

confidence: 57%

Sea-Ice Bacteria Halomonas sp. Strain 363 and Paracoccus sp. Strain 392 Produce Multiple Types of Poly-3-Hydroxyalkaonoic Acid (PHA) Storage Polymers at Low Temperature

Eronen-Rasimus

Hultman

Hải

et al. 2021

Appl Environ Microbiol

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Poly-3-hydroxyalkanoic acids (PHAs) are bacterial storage polymers commonly used in bioplastic production. Halophilic bacteria are industrially interesting organisms as their salinity tolerance and psychrophilic nature lowers sterility requirements and subsequent production costs. We investigated the PHA synthesis in two bacterial strains, Halomonas sp . 363 and Paracoccus sp . 392, isolated from Southern Ocean sea ice and elucidated the related PHA biopolymer accumulation and composition with various approaches, such as transcriptomics, microscopy and chromatography. We show that both bacterial strains produce PHAs at 4°C when the availability of nitrogen and/or oxygen limited growth. The genome of Halomonas sp. 363 encoded three phaC synthase genes and transcribed genes along three PHA pathways (I–III), whereas Paracoccus sp . 392 carry only one phaC gene and transcribed genes along one pathway (I). Thus Halomonas sp. 363 has versatile repertoire of phaC genes and pathways enabling production of both short- and medium chain length PHA products. IMPORTANCE Plastic pollution is one of the most topical threats to the health of the oceans and seas. One recognized way to alleviate the problem is to use degradable bioplastic materials in high-risk applications. PHA is a promising bioplastic material as it is non-toxic and fully produced and degraded by bacteria. Sea ice is an interesting environment for prospecting novel PHA-producing organisms, since traits advantageous to lower production costs, such as tolerance for high salinities and low temperatures are common. We show that two sea-ice bacteria, Halomonas sp. 363 and Paracoccus sp. 392, are able to produce various types of PHA from inexpensive carbon sources. Halomonas sp. 363 is an especially interesting PHA-producing organism, since it has three different synthesis pathways to produce both short- and medium-chain length PHAs.

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Section: Resultssupporting

confidence: 57%

Sea-Ice Bacteria Halomonas sp. Strain 363 and Paracoccus sp. Strain 392 Produce Multiple Types of Poly-3-Hydroxyalkaonoic Acid (PHA) Storage Polymers at Low Temperature

Eronen-Rasimus

Hultman

Hải

et al. 2021

Appl Environ Microbiol

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“…The clustering of cphA and cphB with glycogen synthesis genes suggests that cyanophycin could be an active storage compound for Tetrasphaera . Genes in biosynthetic pathways with increasingly complex metabolites or related functions often cluster together, such as complex electron transport chains ( Simon et al, 2004 ), protection against bacterial host immune response ( Fischbach et al, 2006 ), and intracellular carbon storage ( Kutralam-Muniasamy et al, 2017 ). Further analysis of carbon storage and amino acid utilization in Tetrasphaera can illuminate the role of cyanophycin as a storage compound.…”

Section: Resultsmentioning

confidence: 99%

Meta-omic profiling reveals ubiquity of genes encoding for the nitrogen-rich biopolymer cyanophycin in activated sludge microbiomes

Farmer,

Rajasabhai,

Tarpeh

et al. 2023

Front. Microbiol.

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Recovering nitrogen (N) from municipal wastewater is a promising approach to prevent nutrient pollution, reduce energy use, and transition toward a circular N bioeconomy, but remains a technologically challenging endeavor. Existing N recovery techniques are optimized for high-strength, low-volume wastewater. Therefore, developing methods to concentrate dilute N from mainstream wastewater will bridge the gap between existing technologies and practical implementation. The N-rich biopolymer cyanophycin is a promising candidate for N bioconcentration due to its pH-tunable solubility characteristics and potential for high levels of accumulation. However, the cyanophycin synthesis pathway is poorly explored in engineered microbiomes. In this study, we analyzed over 3,700 publicly available metagenome assembled genomes (MAGs) and found that the cyanophycin synthesis gene cphA was ubiquitous across common activated sludge bacteria. We found that cphA was present in common phosphorus accumulating organisms (PAO) Ca. ‘Accumulibacter’ and Tetrasphaera, suggesting potential for simultaneous N and P bioconcentration in the same organisms. Using metatranscriptomic data, we confirmed the expression of cphA in lab-scale bioreactors enriched with PAO. Our findings suggest that cyanophycin synthesis is a ubiquitous metabolic activity in activated sludge microbiomes. The possibility of combined N and P bioconcentration could lower barriers to entry for N recovery, since P concentration by PAO is already a widespread biotechnology in municipal wastewater treatment. We anticipate this work to be a starting point for future evaluations of combined N and P bioaccumulation, with the ultimate goal of advancing widespread adoption of N recovery from municipal wastewater.

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“…However, this does not explain the almost exclusivity of Class I and II PhaCs to Proteobacteria and the relatively high taxonomic diversity seen in Class III PhaCs. Within the PHA gene cluster, phaC has been identified as the hub gene and plays a major role in cluster formation in prokaryotes ( Kutralam-Muniasamy et al, 2017 ). Further study is required to uncover why Class III PhaC genotypes presumably undergoes more horizontal transfer compared to Class I and II and why Class III cluster appeared to be favored in a higher variety of taxa.…”

Section: Discussionmentioning

confidence: 99%

Developing Bioprospecting Strategies for Bioplastics Through the Large-Scale Mining of Microbial Genomes

et al. 2021

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The accumulation of petroleum-based plastic waste has become a major issue for the environment. A sustainable and biodegradable solution can be found in Polyhydroxyalkanoates (PHAs), a microbially produced biopolymer. An analysis of the global phylogenetic and ecological distribution of potential PHA producing bacteria and archaea was carried out by mining a global genome repository for PHA synthase (PhaC), a key enzyme involved in PHA biosynthesis. Bacteria from the phylum Actinobacteria were found to contain the PhaC Class II genotype which produces medium-chain length PHAs, a physiology until now only found within a few Pseudomonas species. Further, several PhaC genotypes were discovered within Thaumarchaeota, an archaeal phylum with poly-extremophiles and the ability to efficiently use CO2 as a carbon source, a significant ecological group which have thus far been little studied for PHA production. Bacterial and archaeal PhaC genotypes were also observed in high salinity and alkalinity conditions, as well as high-temperature geothermal ecosystems. These genome mining efforts uncovered previously unknown candidate taxa for biopolymer production, as well as microbes from environmental niches with properties that could potentially improve PHA production. This in silico study provides valuable insights into unique PHA producing candidates, supporting future bioprospecting efforts toward better targeted and relevant taxa to further enhance the diversity of exploitable PHA production systems.

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Phylogenetic diversification and developmental implications of poly-(R)-3-hydroxyalkanoate gene cluster assembly in prokaryotes

Cited by 11 publications

References 36 publications

Sea-Ice Bacteria Halomonas sp. Strain 363 and Paracoccus sp. Strain 392 Produce Multiple Types of Poly-3-Hydroxyalkaonoic Acid (PHA) Storage Polymers at Low Temperature

Sea-Ice Bacteria Halomonas sp. Strain 363 and Paracoccus sp. Strain 392 Produce Multiple Types of Poly-3-Hydroxyalkaonoic Acid (PHA) Storage Polymers at Low Temperature

Meta-omic profiling reveals ubiquity of genes encoding for the nitrogen-rich biopolymer cyanophycin in activated sludge microbiomes

Developing Bioprospecting Strategies for Bioplastics Through the Large-Scale Mining of Microbial Genomes

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