From formic acid to single-cell protein: genome-scale revealing the metabolic network of Paracoccus communis MA5

Sheng Tong , Lizhi Zhao , Daling Zhu , Wuxi Chen , Limei Chen , Demao Li

Bioresources and Bioprocessing ›› 2022, Vol. 9 ›› Issue (1) : 55

PDF
Bioresources and Bioprocessing ›› 2022, Vol. 9 ›› Issue (1) : 55 DOI: 10.1186/s40643-022-00544-0
Research

From formic acid to single-cell protein: genome-scale revealing the metabolic network of Paracoccus communis MA5

Author information +
History +
PDF

Abstract

With the increase in population growth and environmental pollution, the daily protein supply is facing great challenges. Single-cell protein (SCP) produced by microorganism fermentation is a good alternative for substituting plant- and animal-derived proteins. In this study, Paracoccus communis MA5 isolated from soil previously demonstrated an excellent ability to synthesize SCP directly from sodium formate. To investigate the central metabolic network of formic acid assimilation and protein synthesis, genome-scale analyses were performed. Genomic analysis showed that complete tetrahydrofolate cycle-, serine cycle-, glycolytic pathway-, tricarboxylic acid (TCA) cycle- and nitrogen metabolism-relevant genes were annotated in the genome. These pathways play key roles in the conversion of formic acid into proteins. Transcriptional analysis showed that sodium formate stress could stimulate the metabolic pathway in response to environmental stress, but weaken the sulfur metabolic pathway to inhibit amino acid synthesis, resulting in a decrease in protein content (30% vs 44%). However, under culture conditions with ammonium sulfate, metabolic pathways associated with protein synthesis were accelerated, causing an increase in protein content (53% vs 44%); while the tetrahydrofolate cycle associated with formic acid assimilation was inhibited, causing a 62.5% decrease in growth rate (OD600: 0.21 vs 0.56). These results provide evidence of protein synthesis from sodium formate in strain MA5 at the gene level and lay a theoretical foundation for the optimization of fermentation systems using formic acid as a carbon source.

Keywords

Formic acid / Single-cell protein / Metabolic network / Genome / Transcriptome / Paracoccus communis

Cite this article

Download citation ▾
Sheng Tong, Lizhi Zhao, Daling Zhu, Wuxi Chen, Limei Chen, Demao Li. From formic acid to single-cell protein: genome-scale revealing the metabolic network of Paracoccus communis MA5. Bioresources and Bioprocessing, 2022, 9(1): 55 DOI:10.1186/s40643-022-00544-0

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Agarwal AS, Zhai Y, Hill D, Sridhar N. The electrochemical reduction of carbon dioxide to formate/formic acid: engineering and economic feasibility. Chemsuschem, 2011, 4(12): 1705-1705.

[2]

Albert J, Luders D, Bsmann A, Guldi DM, Wasserscheid P. Spectroscopic and electrochemical characterization of heteropoly acids for their optimized application in selective biomass oxidation to formic acid. Green Chem, 2014, 16: 226-237.

[3]

Albert J, Wolfel R, Bosmann A, Wasserscheid P. Selective oxidation of complex, water-insoluble biomass to formic acid using additives as reaction accelerators. Energ Environ Sci, 2012, 5(7): 7956-7962.

[4]

Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol, 2010, 11(10): R106.

[5]

Anders S, Pyl PT, Huber W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics, 2015, 31(2): 166-169.

[6]

Attwood MM, Harder W. Formate assimilation by Hyphomicrobium X. FEMS Microbiol Lett, 1978, 3(2): 111-114.

[7]

Awange J, Kiema J. Environmental pollution extreme hydro-climatic and food security challenges: exploiting the Big Data, 2019, Environmental Geoinformatics: Springer, 579-595.

[8]

Bar-Even A, Noor E, Flamholz A. Milo R (2012) Design and analysis of metabolic pathways supporting formatotrophic growth for electricity-dependent cultivation of microbes. BBA Bioenerg, 1827, 89: 1039-1047.

[9]

Bennett A, Lloyd MH, Cuthill IC. Ant-derived formic acid can be toxic for birds. Chemoecology, 1996, 7(4): 189-190.

[10]

Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. Tbtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13(8): 1194-1202.

[11]

Chen W, Liang J, He Z, Jiang W. Preliminary study on total protein extraction methods from Enterococcus faecalis biofilm. Genet Mol Res, 2016

[12]

Chistoserdova L, Kalyuzhnaya MG, Lidstrom ME. The expanding world of methylotrophic metabolism. Annu Rev Microbiol, 2009, 63: 477-499.

[13]

Chistoserdova L. Modularity of methylotrophy, revisited. Environ Microbiol, 2011, 13(10): 2603-2622.

[14]

Crowther GJ, Kosaly G, Lidstrom ME. Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1. J Bacteriol, 2008, 190(14): 5057-5062.

[15]

Enthaler S. Carbon dioxide-the hydrogen-storage material of the future?. Chemsuschem, 2008, 1(10): 801-804.

[16]

Goldberg I, Rock JS, Ben-Bassat A, Mateles RI. Bacterial yields on methanol, methylamine, formaldehyde, and formate. Biotechnol Bioeng, 1976, 18: 1657-1668.

[17]

Jansen K, Thauer RK, Widdel F, Fuchs G. Carbon assimilation pathways in sulfate reducing bacteria Formate, carbon dioxide, carbon monoxide, and acetate assimilation by Desulfovibrio baarsii. Arch Microbiol, 1984, 138(3): 257-262.

[18]

Ji L, Li S, Chen C, Jin H, Wu H, Fan J. Physiological and transcriptome analysis elucidates the metabolic mechanism of versatile Porphyridium purpureum under nitrogen deprivation for exopolysaccharides accumulation. Bioresour Bioprocess, 2021, 8: 73.

[19]

Kim SJ, Yoon J, Im DK, Kim YH, Oh MK. Adaptively evolved Escherichia coli for improved ability of formate utilization as a carbon source in sugar-free conditions. Biotechno Biofuels, 2019, 12(1): 207-218.

[20]

Kopljar D, Inan A, Vindayer P, Wagner N, Klemm E. Electrochemical reduction of CO2 to formate at high current density using gas diffusion electrodes. J Appl Electrochem, 2014, 44(10): 1107-1116.

[21]

Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods, 2012, 9(4): 357-359.

[22]

Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 2009, 25(14): 1754-1760.

[23]

Li Y, Qiu Y, Zhang X, Zhu M, Tan W. Strain screening and optimization of biohydrogen production by Enterobacter aerogenes EB-06 from glycerol fermentation. Bioresour Bioprocess, 2019, 6: 15.

[24]

Lidstrom ME. Aerobic methylotrophic prokaryotes, 2006, The Prokaryotes: Springer, 618-634.

[25]

Liu H, Song T, Fei K, Wang H, Xie J. Microbial electrosynthesis of organic chemicals from CO2 by Clostridium scatologenes ATCC 25775T. Bioresour Bioprocess, 2018, 5: 7.

[26]

Lu X, Leung D, Wang H, Leung M, Xuan J. Electrochemical reduction of carbon dioxide to formic acid. ChemElectroChem, 2014, 1(5): 836-849.

[27]

Lv X, Wu Y, Gong M, Deng J, Gu Y, Liu Y, Li J, Du G, Ledesma-Amaro R, Liu L, Chen J. Synthetic biology for future food: research progress and future directions. Future Foods, 2021

[28]

Marx CJ, Laukel M, Vorholt JA, Lidstrom ME. Purification of the formate-tetrahydrofolate ligase from Methylobacterium extorquens AM1 and demonstration of its requirement for methylotrophic growth. J Bacteriol, 2003, 185(24): 7169-7175.

[29]

Matassa S, Boon N, Pikaar I, Verstraete W. Microbial protein: future sustainable food supply route with low environmental footprint. Microb Biotechnol, 2016, 9(5): 568-575.

[30]

Montanari C, Kamdem SL, Serrazanetti DI, Etoa FX, Guerzoni ME. Synthesis of cyclopropane fatty acids in Lactobacillus helveticus and Lactobacillus sanfranciscensis and their cellular fatty acids changes following short term acid and cold stresses. Food Microbiol, 2010, 27(4): 493-502.

[31]

Morin M, Pierce EC, Dutton R. Changes in the genetic requirements for microbial interactions with increasing community complexity. eLife, 2018, 7: e37072.

[32]

Morris CE. Determination of uracil, uridine and formic acid in egg products by high-performance liquid chromatography. J Chromatogr A, 1987, 394(2): 408-413.

[33]

Myers SS, Smith MR, Guth S, Golden CD, Vaitla B, Mueller ND, . Climate change and global food systems: potential impacts on food security and undernutrition. Annu Rev Publ Health, 2017, 38(1): 259-277.

[34]

Pam IB, Lasika SL, Alicia S, Ann B. Protein demand: review of plant and animal proteins used in alternative protein product development and production. Anim Front, 2020, 10(4): 53-63.

[35]

Pletcher D. The cathodic reduction of carbon dioxide—what can it realistically achieve?. Electrochem Commun, 2015, 61: 97-101.

[36]

Puri A, Bajaj A, Verma H, Kumar R, Singh Y, Lal R. Complete genome sequence of Paracoccus sp. strain AK26: insights into multipartite genome architecture and methylotropy. Genomics, 2020, 112(3): 2572-2582.

[37]

Quivey RG, Faustoferri R, Monahan K, Marquis R. Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans. FEMS Microbiol Lett, 2000, 189(1): 89-92.

[38]

Schrader J, Schilling M, Holtmann D, Sell D, Filho MV, Marx A, Vorholt JA. Methanol-based industrial biotechnology: current status and future perspectives of methylotrophic bacteria. Trends Biotechnol, 2009, 27(2): 107-115.

[39]

Schure ET, Sillje HH, Raeven LJ, Boonstra J, Verkleij AJ, Verrips CT. Nitrogen-regulated transcription and enzyme activities in continuous cultures of Saccharomyces cerevisiae. Microbiology, 1995, 141(5): 1101-1108.

[40]

Shukla RS, Bhatt SD, Thorat RB, Jasra RV. A novel effective hydration of carbon monoxide in liquid phase by a water-soluble ruthenium complex catalyst at moderate pressures in aqueous medium. Appl Catal A-Gen, 2005, 294(1): 111-118.

[41]

Sorokin AB, Kudrik EV, Alvarez LX, Afanasiev P, Millet JM, Bouchu D. Oxidation of methane and ethylene in water at ambient conditions. Catal Today, 2010, 157(1–4): 149-154.

[42]

Spalvins K, Raita S, Valters K, Blumberga D. Improving single cell protein yields and amino acid profile via mutagenesis: review of applicable amino acid inhibitors for mutant selection. Agron Res, 2021, 19(S3): 1285-1307.

[43]

Taheri A, Berben LA. Making C-H bonds with CO2: production of formate by molecular electrocatalysts. Chem Commun, 2016, 52(9): 1759-1767.

[44]

Vorobev A, Jagadevan S, Jain S, Anantharaman K, Dick GJ, Vuilleumier S, Semrau JD. Genomic and transcriptomic analyses of the facultative methanotroph Methylocystis sp. strain SB2 grown on methane or ethanol. Appl Environ Microb, 2014, 80(10): 3044-3052.

[45]

Vuilleumier S, Chistoserdova L, Lee MC, Bringel F, Lajus A, Zhou Y, Gourion B, Barbe V, Chang J, Cruveiller S, Dossat C, Gillett W, Gruffaz C, Haugen E, Hourcade E, Levy R, Mangenot S, Muller E, Nadalig T, Pagni M, Penny C, Peyraud R, Robinson DG, Roche D, Rouy Z, Saenampechek C, Salvignol G, Vallenet D, Wu Z, Marx CJ, Vorholt JA, Olson MV, Kaul R, Weissenbach J, Medigue C, Lidstrom ME. Methylobacterium genome sequences: a reference blueprint to investigate microbial metabolism of C1 compounds from natural and industrial sources. PLoS ONE, 2009, 4(5): e558410.

[46]

Wang Q, Dong H, Yu H. Fabrication of a novel tin gas diffusion electrode for electrochemical reduction of carbon dioxide to formic acid. RSC Adv, 2014, 4(104): 59970-59976.

[47]

Wang WH, Himeda Y, Muckerman JT, Manbeck GF, Fujita E. CO2 Hydrogenation to formate and methanol as an alternative to photo- and electrochemical CO2 reduction. Chem Rev, 2015, 115(23): 12936-12973.

[48]

Wolfel R, Taccardi N, Bosmann A, Wasserscheid P. Selective catalytic conversion of biobased carbohydrates to formic acid using molecular oxygen. Green Chem, 2011, 13(10): 2759-2763.

[49]

Xu R, Deng WSY, Jiang WH, Gu Y. Progress in biological utilization of formic acid. Chin J Biotechnol, 2020, 36(6): 1031-1040.

[50]

Yishai O, Goldbach L, Tenenboim H, Lindner SN, Bar-Even A. Engineered assimilation of exogenous and endogenous formate in Escherichia coli. Acs Synth Biol, 2017, 6(9): 1722-1731.

[51]

Zhao L, Zhu D, Li D. Screening and fermentation process of single cell protein-producing strains by formic acid. Feed Res, 2021, 44(9): 88-93. in Chinese

Funding

National Key R&D Programs of China(2018YFA090048)

Tianjin Synthetic Biotechnology Innovation Capacity Improvement Project(TSBICIP-KJGG-004-21)

Tianjin Synthetic Biotechnology Innovation Capacity Improvement Project (TSBICIP-CXRC-050)

AI Summary AI Mindmap
PDF

128

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/