Enhanced eicosapentaenoic acid production by a new deep-sea marine bacterium Shewanella electrodiphila MAR441T

Zhang, Jinwei; Burgess, J. Grant

doi:10.1371/journal.pone.0188081

Cited by 16 publications

(12 citation statements)

References 70 publications

(86 reference statements)

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“…Given the presence of two discrete pathways for the biosynthesis of unsaturated fatty acids, we hypothesized that genes critical for MUFA synthesis could be disrupted in the native producing organism and compensated for by PUFA produced by the Pfa synthase. Previous work utilizing the fatty acid biosynthesis inhibitor cerulenin ( 7 , 20 ) or genetic disruption of the fabF gene, which encodes the key condensing enzyme, β-ketoacyl-ACP (acyl carrier protein) synthase II, involved in 18:1 production ( 9 ), showed that compensatory increases in PUFA content mitigated the loss of MUFA biosynthesis in the marine bacterium Photobacterium profundum SS9. Additionally, transposon screening for pressure-sensitive mutants of P. profundum SS9 revealed that fabB was not an essential gene and that its disruption led to a pressure-sensitive phenotype ( 21 ).…”

Section: Introductionmentioning

confidence: 99%

Genetic Suppression of Lethal Mutations in Fatty Acid Biosynthesis Mediated by a Secondary Lipid Synthase

Allemann

Allen

2021

Appl Environ Microbiol

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The biosynthesis and incorporation of polyunsaturated fatty acids into phospholipid membranes is a unique feature of certain marine Gammaproteobacteria inhabiting high-pressure and/or low temperature environments. In these bacteria, monounsaturated and saturated fatty acids are produced via the classical dissociated Type II fatty acid synthase mechanism, while omega-3 polyunsaturated fatty acids such as EPA (20:5n-3) and DHA (22:6n-3) are produced by a hybrid polyketide/fatty acid synthase – encoded by the pfa genes - also referred to as the secondary lipid synthase mechanism. In this work, phenotypes associated with partial or complete loss of monounsaturated biosynthesis are shown to be compensated for by several-fold increased production of polyunsaturated fatty acids in the model marine bacterium Photobacterium profundum SS9. One route to suppression of these phenotypes could be achieved by transposition of insertion sequences within or upstream of the fabD, malonyl CoA-acyl carrier protein transacylase, coding sequence. Genetic experiments in this strain indicated that fabD is not an essential gene, yet mutations in fabD and pfaA are synthetically lethal. Based on these results, we speculated that the malonyl-CoA transacylase domain within PfaA compensates for loss of FabD activity. Heterologous expression of either pfaABCD from P. profundum SS9 or pfaABCDE from Shewanella pealeana in Escherichia coli complemented the loss of the chromosomal copy of fabD in vivo. The co-occurrence of independent, yet compensatory fatty acid biosynthetic pathways in select marine bacteria may provide genetic redundancy to optimize fitness under extreme conditions. Importance A defining trait among many cultured piezophilic and/or psychrophilic marine Gammaproteobacteria is the incorporation of both monounsaturated and polyunsaturated fatty acids into membrane phospholipids. The biosynthesis of these different classes of fatty acid molecules is linked to two genetically distinct co-occurring pathways that utilize the same pool of intracellular precursors. Using a genetic approach, new insights have been gained into the interactions between these two biosynthetic pathways. Specifically, core fatty acid biosynthesis genes previously thought to be essential were found to be non-essential in strains harboring both pathways due to functional overlap between the two pathways. These results provide new routes to genetically optimize long-chain omega-3 polyunsaturated fatty acid biosynthesis in bacteria and reveal a possible ecological role for maintaining multiple pathways for lipid synthesis in a single bacterium.

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Section: Introductionmentioning

confidence: 99%

Genetic Suppression of Lethal Mutations in Fatty Acid Biosynthesis Mediated by a Secondary Lipid Synthase

Allemann

Allen

2021

Appl Environ Microbiol

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“…This result is consistent with the study of Dailey et al (), wherein the authors recovered numerous red bacterial colonies on TTC plates while plating the broth cultures of fish intestine samples. The highest TPC and putative omega‐3 producers were recorded for samples collected from station K6 with a depth of 11 m. Generally, omega‐3 fatty acid producing bacteria were predominately isolated from sediment and fish intestines samples collected from Ocean depths (Akimoto et al, ; Bianchi et al, ; Zhang and Burgess, ); however, reports of isolation from shallow temperate waters are also available (Shulse and Allen, ). In this study from subtropical area, the putative omega‐3 producers count were higher in samples collected at 11 m than at 32 m depth.…”

Section: Resultsmentioning

confidence: 99%

“…The reported levels in the present study also fall into mid‐ or low‐level category. Several authors have attempted to optimize the media and growth conditions and reported higher levels of EPA up to 40% of TFAs at the standardized conditions (Akimoto et al, ; Yazawa, ; Cho and Mo, ; Zhang and Burgess, ). Hence, a detailed molecular characterization is required to find out the mechanism of EPA production by these isolates which were negative for all three of these genes.…”

Section: Resultsmentioning

confidence: 99%

“…Since 2000, world’s fish stocks are declining, and hence, scientists are exploring the alternative inexpensive and safe source of omega‐3 fatty acids (Hinzpeter et al, ). Recent researches have shown that the marine bacteria isolated from sediment and intestines of marine fish could be an alternative and abundant source of omega‐3 fatty acids either by natural production or through genetic engineering (Hirota et al, ; Shulse and Allen, ; Amiri‐Jami et al, ; Dailey et al, ; Zhang and Burgess, ). PUFA producers were mainly isolated from polar and deep‐sea regions (Bowman et al, ; Hirota et al, ; Shulse and Allen, ; Bianchi et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Isolation of Gram‐positiveFirmibacteriaas major eicosapentaenoic acid producers from subtropical marine sediments

Surendraraj

Farvin

Fakhraldeen

et al. 2019

Lett Appl Microbiol

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In this study, a total of 172 putative omega‐3 producers were isolated from 28 sediment samples from the Arabian Gulf employing a selective isolation procedure using marine agar containing 0·1% triphenyl tetrazolium chloride (TTC). Out of these 172 isolates, 19 isolates produced eicosapentaenoic acid (EPA) as confirmed by Gas Chromatography‐Mass Spectrometry (GC‐MS). The EPA content of the isolated bacterial strain varied from 1·76 to 6·52% of total fatty acids. Among the 19 isolates of EPA producers, while 17 isolates harboured both pfaA gene and Δ6 desaturase gene, only five isolates harboured Δ5 desaturase gene. Two of the EPA positive strains harbour none of the three genes tested. The 16s RNA identification of these isolates revealed that except one, all the EPA producers were Gram‐positive marine bacteria belonging to the phylum Firmicutes, family Bacillacea, genera Bacillus and Oceanobacillus. Halomonas pacifica was the only Gram‐negative Gamma‐Proteobacteria detected to produce EPA from this region. Significance and Impact of the Study Recently, marine bacteria are considered as a promising source of polyunsaturated fatty acid (PUFA) over marine fishes and microalgae. PUFA producers reported from polar and deep‐sea sources were restricted to five well‐known marine genera under two distinct domains of bacteria such as proteobacteria (Shewanella, Colwellia, and Moritella) and cytophaga group (Flexibacter, Psychroflexus). This study revealed that subtropical marine environment could also be the source of PUFA producing bacteria, and they predominantly belonged to the class of Firmibacteria. This finding opens up new avenue for research to study the inherent mechanism and physiology of such organisms from this unique environment.

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“…Certain barophilic and psychrophilic organisms found in the ocean depths, such as members of the Shewanella genus, have been demonstrated to be substantial PUFA producers ( 133 ). Shewanella electrodiphila MAR441 was found to produce more EPA after being supplemented with cerulenin (FAS inhibitor) ( 134 ). In Shewanella species PKS-like gene clusters were identified for EPA biosynthesis that was successfully expressed in E. coli to produce EPA ( 135 ).…”

Section: Metabolic Engineering Of Existing Microbesmentioning

confidence: 99%

Microbes: A Hidden Treasure of Polyunsaturated Fatty Acids

et al. 2022

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Microbes have gained a lot of attention for their potential in producing polyunsaturated fatty acids (PUFAs). PUFAs are gaining scientific interest due to their important health-promoting effects on higher organisms including humans. The current sources of PUFAs (animal and plant) have associated limitations that have led to increased interest in microbial PUFAs as most reliable alternative source. The focus is on increasing the product value of existing oleaginous microbes or discovering new microbes by implementing new biotechnological strategies in order to compete with other sources. The multidisciplinary approaches, including metabolic engineering, high-throughput screening, tapping new microbial sources, genome-mining as well as co-culturing and elicitation for the production of PUFAs, have been considered and discussed in this review. The usage of agro-industrial wastes as alternative low-cost substrates in fermentation for high-value single-cell oil production has also been discussed. Multidisciplinary approaches combined with new technologies may help to uncover new microbial PUFA sources that may have nutraceutical and biotechnological importance.

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Enhanced eicosapentaenoic acid production by a new deep-sea marine bacterium Shewanella electrodiphila MAR441T

Cited by 16 publications

References 70 publications

Genetic Suppression of Lethal Mutations in Fatty Acid Biosynthesis Mediated by a Secondary Lipid Synthase

Genetic Suppression of Lethal Mutations in Fatty Acid Biosynthesis Mediated by a Secondary Lipid Synthase

Isolation of Gram‐positiveFirmibacteriaas major eicosapentaenoic acid producers from subtropical marine sediments

Microbes: A Hidden Treasure of Polyunsaturated Fatty Acids

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