Formatotrophs

Formatotrophs are organisms that can assimilate formate or formic acid to use as a carbon source or for reducing power.[1] Some authors classify formatotrophs as one of the five trophic groups of methanogens, which also include hydrogenotrophs, acetotrophs, methylotrophs, and alcoholotrophs.[2] Formatotrophs have garnered attention for applications in biotechnology as part of a "formate bioeconomy" in which synthesized formate could be used as a nutrient for microoganisms.[3][4] Formate can be electrochemically synthesized from CO2 and renewable energy, and formatotrophs may be genetically modified to enhance production of biochemical products to be used as biofuels. Technical limitations in culturing formatotrophs have limited the discovery of natural formatotrophs and impeded research on their formate-metabolizing enzymes, which are of interest for applications in carbon sequestration and astrobiology.

Etymology

Formatotrophs gain their name from Latin formica, meaning "ant"[5] (formic acid having been named for its presence as a chemical defense in ants) and from Greek trophikos, meaning "pertaining to nourishment or food."[6]

Natural formatotrophs and their ecological role

Formatotrophs perform key metabolic processes through syntrophic relationships. In these relationships, formate is harvested for energy or carbon metabolism in diverse environments. These reactions are of particular importance in biogeochemical process related to carbon cycling and transfer of reducing agents such as hydrogen, acting as a keystone with abiotic formate.[7] Some methanogenic organisms convert formate into hydrogen and bicarbonate, providing hydrogen for other methanogens. Formate can be assimilated by formatotrophs in syntrophic associations with methanogens present during oxidation of formate; otherwise, formate oxidation would not be energetically sufficient to support growth and is thermodynamically disfavored (△G = +1.3 kJ /mol). So at least one methanogenic partner microorganism must be present to remove hydrogen. Some microorganisms, such as Desulfurococcus amylolyticus, are able to convert formate into carbon dioxide, acetate, citrate, and ethanol.[8]

Formate oxidation equation

Examples of natural formatotrophs

Confocal laser scanning microscopy images showing different microbial morphotypes in chimney samples from the Lost City hydrothermal field[13]

Recent metagenomic studies indicate widespread presence of potential formatotrophs in the Lost City hydrothermal field, an area of alkaline hydrothermal chimneys in the Atlantic Ocean, where serpentinization reactions of rock matter form calcium carbonate structures, hydrogen, methane, formate and other components. The exteriors of the chimneys are usually coated in biofilm.[13][14] Harsh environmental conditions limit the development of microorganisms because chemical reactions keep concentrations of dissolved inorganic carbon low, indicating that carbon dioxide is not the primary carbon source.[15] Thus, initial studies hypothesized that formate was the main carbon source due the high concentrations of formate (36 to 158 μM) found in the field.[16] The metabolism of microbial communities in the hydrothermal field are largely unknown due to difficulties with laboratory isolation and culture. Metagenomic and genomic evidence supports the assimilation of formate in the Lost City chimneys as the main carbon source.[17] Metagenome assembled genomes (MAGs) determined that the most abundant genome was in the Methanosarcinales, which did not present metabolic pathways related with formate metabolism, and Chloroflexis MAGs were five times less abundant.

The biofilm formed over the chimneys in the Lost City provides a glimpse of one possible carbon cycle that may have been in operation in the early days of life on earth, in an ecosystem based on geochemical reactions.[18] Similarly, studies of carbon assimilation strategies in ultrabasic groundwater explored the chemosynthesis microbial reactions in wells drilled into the ultramafic Coast Range Ophiolite Microbial Observatory (CROMO) and found that the microbial communities present in those aquifers use the products of serpentinization, including formate and methane, as carbon sources.

C. necator is one of the most well-studied aerobic formatotrophs. It can use carbon dioxide, formate, and hydrogen as carbon and energy sources and has a denitrification process. It is a model microorganism studied for production of polyhydroxyalkanoate, a compound of interest in bioplastic engineering. It has been gaining particular attention to be used as a chassis for metabolic engineering for the synthesis of alcohols and other bio-based compounds. A significant limitation for further engineering with this strain is the limited cell density that can be achieved in chemically defined media.

Carbon production in the Lost City hydrothermal field. Formate is converted to CO2 by sulfate reducers and then consumed by autotrophs such as Methanosarcinales.[15]

Formate assimilation metabolic pathways

Natural metabolic pathways for formate assimilation include the reductive pentose phosphate pathway, serine pathway, reductive acetyl-CoA pathway in acetogens, reductive acetyl-CoA pathway in methanogens, and glycine pathway. The reductive pentose phosphate pathway uses 11 formate molecules to produce 1 acetyl-CoA, whereas the reductive acetyl-CoA pathway uses only 4.

Table 1: Summary of metabolic pathways for formate assimilation
Pathway Amount of formate required to synthesize acetyl-CoA
Reductive pentose phosphate pathway 11 formate molecules (4 for NADPH regeneration and 7 for ATP production)
Serine pathway 7 formate molecules (1 assimilated, 3 to provide NADPH, and 3 for ATP generation)
Reductive acetyl-CoA pathway in acetogens and methanogens 4 formate molecules (1 assimilated, 3 to provide NADPH)

Formatotrophs for carbon sequestration

The low ionization potential of formate makes it a good electron donor to provide reducing power to microorganisms. To sequester carbon, the production of formate by electrosynthesis — an abiotic process — could be integrated with a biotic process that uses it as a carbon source. Formatotrophic microorganism could feasibly be used to produce valuable chemicals.[10] Few formatotrophs have been studied, and thus most research into fermentation of formate is focused on the development of synthetic pathways or matching enzymes from different microorganism to create totally new pathways[19] and on the improvement of enzymes by directed evolution techniques. There are many pathways that could potentially assimilate formate for the production of biofuels, other biosynthetic products or single-cell protein, whether by using existing formate-fixing reactions or by designing novel enzymes.[20]

The US Department of Energy, US National Renewable Energy Laboratory and US Advanced Research Projects Agency–Energy have set up funding opportunities to improve formate assimilation with C. necator.[21]

Microorganism growing in serpentinization systems are of interest to understand carbon cycling between abiotic and biotic systems. These studies have further applications in astrobiology and studies of evolution and the emergence of life.

References

  1. ↑ Fabarius JT, Wegat V, Roth A, Sieber V (April 2021). "Synthetic Methylotrophy in Yeasts: Towards a Circular Bioeconomy". Trends in Biotechnology. 39 (4): 348–358. doi:10.1016/j.tibtech.2020.08.008. PMID 33008643. S2CID 222143629.
  2. ↑ Barbera AC, Vymazal J, Maucieri C (2019). "Greenhouse gases formation and emission.". Encyclopedia of Ecology. Vol. 2 (Second ed.). pp. 329–333. doi:10.1016/B978-0-12-409548-9.10895-4. ISBN 9780444641304. S2CID 133696333.
  3. ↑ Bar-Even A (22 March 2016). "Synthetic metabolism and the formate bio-economy concept:addressing humanity's grand challenges". Imperial College London. Retrieved 2021-11-18.
  4. ↑ Kensy F, Formate Bioeconomy – A new way for sustainable biomanufacturing?, retrieved 2021-11-18
  5. ↑ "Formica". Online Etymology Dictionary. Retrieved 2021-12-22.{{cite web}}: CS1 maint: url-status (link)
  6. ↑ "Trophus". Online Etymology Dictionary. Retrieved 2021-12-22.{{cite web}}: CS1 maint: url-status (link)
  7. ↑ Morris BE, Henneberger R, Huber H, Moissl-Eichinger C (May 2013). "Microbial syntrophy: interaction for the common good". FEMS Microbiology Reviews. 37 (3): 384–406. doi:10.1111/1574-6976.12019. PMID 23480449.
  8. 1 2 Ergal I, Reischl B, Hasibar B, Manoharan L, Zipperle A, Bochmann G, et al. (March 2020). "Formate Utilization by the Crenarchaeon Desulfurococcus amylolyticus". Microorganisms. 8 (3): 454. doi:10.3390/microorganisms8030454. PMC 7143981. PMID 32210133.
  9. ↑ Carere CR, Hards K, Wigley K, Carman L, Houghton KM, Cook GM, Stott MB (2021). "Growth on Formic Acid Is Dependent on Intracellular pH Homeostasis for the Thermoacidophilic Methanotroph Methylacidiphilum sp. RTK17.1". Frontiers in Microbiology. 12: 651744. doi:10.3389/fmicb.2021.651744. PMC 8024496. PMID 33841379.
  10. 1 2 Yishai O, Lindner SN, Gonzalez de la Cruz J, Tenenboim H, Bar-Even A (December 2016). "The formate bio-economy". Current Opinion in Chemical Biology. Energy Mechanistic Biology. 35: 1–9. doi:10.1016/j.cbpa.2016.07.005. PMID 27459678.
  11. ↑ Bae SS, Kim TW, Lee HS, Kwon KK, Kim YJ, Kim MS, et al. (January 2012). "H2 production from CO, formate or starch using the hyperthermophilic archaeon, Thermococcus onnurineus". Biotechnology Letters. 34 (1): 75–79. doi:10.1007/s10529-011-0732-3. PMID 21898132. S2CID 13057806.
  12. ↑ Crowther GJ, Kosály G, Lidstrom ME (July 2008). "Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1". Journal of Bacteriology. 190 (14): 5057–5062. doi:10.1128/JB.00228-08. PMC 2447001. PMID 18502865.
  13. 1 2 Lecoeuvre A, Ménez B, Cannat M, Chavagnac V, Gérard E (March 2021). "Microbial ecology of the newly discovered serpentinite-hosted Old City hydrothermal field (southwest Indian ridge)". The ISME Journal. 15 (3): 818–832. doi:10.1038/s41396-020-00816-7. PMC 8027613. PMID 33139872.
  14. ↑ Lang SQ, Brazelton WJ (February 2020). "Habitability of the marine serpentinite subsurface: a case study of the Lost City hydrothermal field". Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences. 378 (2165): 20180429. Bibcode:2020RSPTA.37880429L. doi:10.1098/rsta.2018.0429. PMC 7015304. PMID 31902336.
  15. 1 2 Lang SQ, Früh-Green GL, Bernasconi SM, Brazelton WJ, Schrenk MO, McGonigle JM (January 2018). "Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field". Scientific Reports. 8 (1): 755. Bibcode:2018NatSR...8..755L. doi:10.1038/s41598-017-19002-5. PMC 5768773. PMID 29335466.
  16. ↑ McGonigle JM, Lang SQ, Brazelton WJ (April 2020). "Genomic Evidence for Formate Metabolism by Chloroflexi as the Key to Unlocking Deep Carbon in Lost City Microbial Ecosystems". Applied and Environmental Microbiology. 86 (8): e02583–19. doi:10.1128/AEM.02583-19. PMC 7117926. PMID 32033949.
  17. ↑ McGonigle JM, Lang SQ, Brazelton WJ (April 2020). "Genomic Evidence for Formate Metabolism by Chloroflexi as the Key to Unlocking Deep Carbon in Lost City Microbial Ecosystems". Applied and Environmental Microbiology. 86 (8). doi:10.1128/AEM.02583-19. PMC 7117926. PMID 32033949.
  18. ↑ "NOAA Ocean Explorer". oceanexplorer.noaa.gov. Retrieved 2021-11-18.
  19. ↑ Mao W, Yuan Q, Qi H, Wang Z, Ma H, Chen T (August 2020). "Recent progress in metabolic engineering of microbial formate assimilation". Applied Microbiology and Biotechnology. 104 (16): 6905–6917. doi:10.1007/s00253-020-10725-6. PMID 32566995. S2CID 219958811.
  20. ↑ Bar-Even A (July 2016). "Formate Assimilation: The Metabolic Architecture of Natural and Synthetic Pathways". Biochemistry. 55 (28): 3851–3863. doi:10.1021/acs.biochem.6b00495. PMID 27348189.
  21. ↑ Johnson CW (2021-03-15). "BETO 2021 Peer Review - Improving Formate Upgrading by Cupriavidus Necator 2.3.2.111". OSTI 1772964. {{cite journal}}: Cite journal requires |journal= (help)
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