Biology:Hydrogen oxidizing bacteria

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Hydrogen oxidizing bacteria are a group of facultative autotrophs that can use hydrogen as an electron donor. They can be divided into aerobes and anaerobes. The former use hydrogen as an electron donor and oxygen as an acceptor while the latter use sulphate or nitrogen dioxide as electron acceptors.[1] Some species of both bacteria types have been isolated in different environments, for example in fresh waters, sediments, soils, activated sludge, hot springs, hydrothermal vents and percolating water.[2]

These organisms are able to exploit the special properties of molecular hydrogen (for instance redox potential and diffusion coefficient) thanks to the presence of hydrogenases.[3] The aerobic hydrogen oxidizing bacteria are facultative autotrophs, but they can also have mixotrophic or completely heterotrophic growth. Most of them show greater growth on organic substrates. The use of hydrogen as an electron donor coupled with the ability to synthesize organic matter, through the reductive assimilation of CO2, characterize the hydrogen oxidizing bacteria. Among the most represented genres of these organisms we find: Caminibacter, Aquifex, Ralstonia and Paracoccus.

Sources of hydrogen

The most widespread element on our Earth is hydrogen, which represents around three-quarters of all the elements.[4] In the atmosphere, its concentration is about 0.5-0.6 ppm and so here it represents the most abundant trace gas, after methane.[3] Therefore, H2 can be used as energy source in several biological processes, also because it has a highly negative redox potential (E0’= -0.414 V) . It can be coupled with different compounds:

-       O2: the oxic respiration is performed (H2+1/2O2 → H2O)

-       Oxidized compounds, such as carbon dioxide or sulfate.[5]

In the ecosystems, hydrogen can be produced through biological and abiotic processes .

The abiotic processes are mainly due to geothermal production[6] and serpentinization.[7] In the first case, hydrogen is usually present as a gas and probably can be obtained by different reactions:

1.      Water may react with silicon radical at high temperature:

Si· + H2O → SiOH + H·

H· + H· → H2

2.      The proposed reaction between iron oxides and water, at temperatures higher than 800 °C:

2FeO + H2O → Fe2O3 + H2

2Fe3O4 + H2O → 3Fe2O3 + H2 [6]

On the other hand, serpentinization is an exothermic geochemical mechanism that occurs when, thanks to the tectonic movements, the ultramafic rocks raise and reach the water. This process can bring to the production of large quantities of H2, but also of methane and organic substances.[7]

The main mechanisms that lead to the formation of hydrogen, involving different microorganisms, are nitrogen fixation and fermentation. The first one happens in some bacteria, such as heterocystous and non-heterocystous cyanobacteria, that have a specialized enzyme, the nitrogenase, which catalizes the reduction of N2 to NH4+. In addition, these microorganisms have another enzyme, the hydrogenase, that oxidizes the H2 released as a by-product.[4] Therefore, in this type of bacteria, the amount of hydrogen produced depends on the ratio between H2 production and consumption.[8] In some cases, the H2 can be present in the environments because the N2-fixing bacteria can have a low quantity of hydrogenases.[9][8] Instead, fermentation is performed by some strict or facultative anaerobic heterotrophic bacteria, in particular Clostridia,[10] that degrade organic molecules, producing hydrogen as one of the products. Therefore, this type of metabolism mainly occurs in anoxic sites, such as lake sediments, deep-sea hydrothermal vents and human gut.[11]

Probably mainly due to the biotic processes, in the marine habitats it was observed that the concentrations of hydrogen were supersaturated. In all these environments, the highest concentrations were in the first metres, decreasing to the thermocline and reaching the lowest concentrations in the deep oceans.[3] Globally, tropical and subtropical oceans appear to have the most abundant quantity of H2,[12][3][13] while the least amount is present in higher latitudes[3][14][15] However, it was observed that the release of hydrogen in the oceans is dependent on the solar radiation, showing a daily change with the maximum peak at noon.[3][12][13] Nitrogen fixation, performed by cyanobacteria, leads to the production of one molecule of H2 at least. This metabolism is thought to be the major one involved in the increase of H2 in the oceans .[3] Despite there are some evidences of this,[16][17] more data need to be collected to finally correlate the two phenomena.

Examples

Hydrothermal vent

H2 is an important electron donor in a particular environment: Hydrothermal vents. In this environment hydrogen oxidation represents a significant origin of energy, sufficient to conduct ATP synthesis and autotrophic CO2 fixation so hydrogen oxidizing bacteria are relevant in deep sea habitats. Among the main chemosynthetic reactions that take place in hydrothermal vents, the oxidation of the sulphide and the hydrogen one covers a central role. In particular, for autotrophic carbon fixation, hydrogen oxidation metabolism is more favored than the sulfide/thiosulfate oxidation, although less energy is released (only -237 kJ/mol compared to – 797 kJ/mol).[18] To fix a mole of carbon during the hydrogen oxidation, one third of the energy necessary for the sulphide oxidation is used. This is due to the redox potential of hydrogen, which is more negative than NAD (P)/H. Based on the amount of sulphide, hydrogen and other farm biotics, this phenomenon can be intensified leading, in some cases, to an energy production by oxidation of the hydrogen of 10 -18 times higher than produced one by the sulphide oxidation.[19][20]

Knallgas bacteria

Aerobic hydrogen oxidizing bacteria, sometimes called Knallgas bacteria, are bacteria that oxidize hydrogen with oxygen as final electron acceptor. See microbial metabolism (hydrogen oxidation). These bacteria include Hydrogenobacter thermophilus, Cupriavidus necator, and Hydrogenovibrio marinus. There are both Gram positive and Gram negative Knallgas bacteria.

Most grow best under microaerobic conditions because the hydrogenase enzyme used in hydrogen oxidation is inhibited by the presence of oxygen, but oxygen is still needed as a terminal electron acceptor and energy source.[21]

The word Knallgas means "oxyhydrogen" (a mixture of hydrogen and oxygen, literally "bang-gas") in German.

Strain MH-110

Ocean’s surface water is characterized by a high concentration of hydrogen.[22] In 1989, for the first time, an aerobic hydrogen oxidizing bacteria was isolated from sea water and the discovery of this strain was very important also because for the first time a hydrogen oxidizing bacteria was identified in normal temperature conditions. Experimentally it has been shown that the MH-110 strain is able to grow in an atmosphere (under a continuous gas flow system) characterized by an oxygen concentration of 40% (analogous characteristics are present in the surface water from which the bacteria were isolated, which is, in fact, a fairly aerated medium). This differs from the usual behaviour of hydrogen oxidizing bacteria, which in general thrive strictly under microaerophilic conditions (<10% O2).[23][24]

This strain is also capable of coupling the hydrogen oxidation with the reduction of sulfur compounds such as thiosulfate and tetrathionate.

Metabolism

Knallgas bacteria are a group of bacteria which are able to fix carbon dioxide using H2 as their chemical energy source. Knallgas bacteria stand out from other hydrogen oxidizing bacteria which, although using H2 as energy source, are not able to fix CO2, as Knallgas do.[25]

This aerobic hydrogen oxidation, also known as the Knallgas reaction, which releases a considerable amount of energy, determines the generation of a proton motive force (PMF):

H2 + O2 [math]\displaystyle{ \longrightarrow }[/math] H2O ΔGo = -237 kJ/mol

The key enzymes involved in this reaction are the hydrogenases which lead the electrons through the electron transport chain, from hydrogen to the final acceptor, that is O2 which is actually reduced to water, the only product.[26] The hydrogenases, which are divided into three categories according to the type of metal present in the active site, are the enzymes that allow the oxidation of hydrogen. The first evidence of the presence of these enzymes was found in Pseudomonas saccharophila, Alcaligenes ruhlandii and Alcaligenese eutrophus, in which there are two types of hydrogenases: cytoplasmatic and membrane-bound. While the first enzyme takes up hydrogen and reduces NAD+ to NADH for carbon fixation, the second is involved in the generation of the proton motive force.[27][28] In most Knallgas bacteria only one type of hydrogenase was observed, the one bound to the membrane that provided hydrogen activation.[29]

While these microorganisms are also defined as facultative autotrophs, some are also able to live in completely heterotrophic conditions using organic substances as electron donors; in this case, the hydrogenase activity is less important or completely absent.[1]

However, Knallgas bacteria, growing as chemolithoautotrophs, as soon as they integrate a molecule of CO2 can produce, through the Calvin Benson Cycle or reverse citric acid cycle (TCA cycle), biomolecules necessary for the cell:[30][31]

6H2 + 2O2 + CO2 [math]\displaystyle{ \longrightarrow }[/math] (CH2O) + 5H2O

A recent study of Alcaligenes eutropha, one of the most representative species of Knallgas bacteria, highlighted that at low concentrations of O2 (about 10 mol %) and consequently with a low ΔH2/ΔCO2 molar ratio (3.3), the energy efficiency of CO2 fixation increases until 50%. This is an interesting characteristic of these microorganisms because once assimilated, carbon dioxide is reduced to polyhydroxybutyrate, whose derivatives, being biodegradable, are used in various eco-sustainable applications.[32][33]

Uses

Given enough nutrients, H2, O2 and CO2, many knallgas bacteria can be grown very quickly in vats using only a small amount of area. This makes it possible to cultivate them as an environmentally sustainable source of food and other products.

Solar Foods is a startup that has sought to commercialize this, using renewable energy to split hydrogen to grow a neutral tasting protein-rich food source for use in products such as artificial meat.[34] Independent studies have also shown that knallgas cultivation is more environmentally friendly than traditional crops.[35]

References

  1. ↑ 1.0 1.1 Aragno, Michel; Schlegel, Hans G. (1981). "The Hydrogen-Oxidizing Bacteria". in Starr, Mortimer P.; Stolp, Heinz; Trüper, Hans G. et al.. The Prokaryotes. Berlin, Heidelberg: Springer. pp. 865–893. doi:10.1007/978-3-662-13187-9_70. ISBN 978-3-662-13187-9. 
  2. ↑ "Ethanol and hydrogen production by two thermophilic, anaerobic bacteria isolated from Icelandic geothermal areas". Biotechnology and Bioengineering 101 (4): 679–90. November 2008. doi:10.1002/bit.21942. PMID 18500766. 
  3. ↑ 3.0 3.1 3.2 3.3 3.4 3.5 3.6 "Distribution analysis of hydrogenases in surface waters of marine and freshwater environments". PLOS ONE 5 (11): e13846. November 2010. doi:10.1371/journal.pone.0013846. PMID 21079771. Bibcode: 2010PLoSO...513846B. 
  4. ↑ 4.0 4.1 "Hydrogen production by biological processes: a survey of literature". International Journal of Hydrogen Energy 26 (1): 13–28. January 2001. doi:10.1016/S0360-3199(00)00058-6. 
  5. ↑ "Energetic constraints on H2-dependent terminal electron accepting processes in anoxic environments: a review of observations and model approaches". Environmental Science & Technology 44 (1): 24–33. January 2010. doi:10.1021/es9018207. PMID 20039730. Bibcode: 2010EnST...44...24H. 
  6. ↑ 6.0 6.1 Aragno, Michel (1992). "Thermophilic, Aerobic, Hydrogen-Oxidizing (Knallgas) Bacteria". in Balows, Albert; Trüper, Hans G.; Dworkin, Martin et al. (in en). The Prokaryotes. New York: Springer. pp. 3917–3933. doi:10.1007/978-1-4757-2191-1_55. ISBN 978-1-4757-2191-1. 
  7. ↑ 7.0 7.1 "Metagenomic evidence for h(2) oxidation and h(2) production by serpentinite-hosted subsurface microbial communities". Frontiers in Microbiology 2: 268. 2012. doi:10.3389/fmicb.2011.00268. PMID 22232619. 
  8. ↑ 8.0 8.1 Tiwari, Archana; Pandey, Anjana (January 2012). "Cyanobacterial hydrogen production – A step towards clean environment". International Journal of Hydrogen Energy 3 7 (1): 139–150. doi:10.1016/j.ijhydene.2011.09.100. 
  9. ↑ "Cultivation-independent detection of autotrophic hydrogen-oxidizing bacteria by DNA stable-isotope probing". Applied and Environmental Microbiology 77 (14): 4931–8. July 2011. doi:10.1128/aem.00285-11. PMID 21622787. Bibcode: 2011ApEnM..77.4931P. 
  10. ↑ "Biological hydrogen production: not so elementary". Science 282 (5395): 1842–3. December 1998. doi:10.1126/science.282.5395.1842. PMID 9874636. 
  11. ↑ "Microbially Mediated Hydrogen Cycling in Deep-Sea Hydrothermal Vents". Frontiers in Microbiology 9: 2873. 2018. doi:10.3389/fmicb.2018.02873. PMID 30532749. 
  12. ↑ 12.0 12.1 Herr, Frank L.; Frank, Ernest C.; Leone, Gerald M.; Kennicutt, Mahlon C. (January 1984). "Diurnal variability of dissolved molecular hydrogen in the tropical South Atlantic Ocean". Deep Sea Research Part A. Oceanographic Research Papers 31 (1): 13–20. doi:10.1016/0198-0149(84)90069-4. Bibcode: 1984DSRA...31...13H. 
  13. ↑ 13.0 13.1 Conrad, Ralf; Seiler, Wolfgang (December 1988). "Methane and hydrogen in seawater (Atlantic Ocean)". Deep Sea Research Part A. Oceanographic Research Papers 35 (12): 1903–1917. doi:10.1016/0198-0149(88)90116-1. Bibcode: 1988DSRA...35.1903C. 
  14. ↑ Herr, Frank L.; Scranton, Mary I.; Barger, William R. (September 1981). "Dissolved hydrogen in the Norwegian Sea: Mesoscale surface variability and deep-water distribution". Deep Sea Research Part A. Oceanographic Research Papers 28 (9): 1001–1016. doi:10.1016/0198-0149(81)90014-5. ISSN 0198-0149. Bibcode: 1981DSRA...28.1001H. 
  15. ↑ Punshon, Stephen; Moore, Robert M.; Xie, Huixiang (April 2007). "Net loss rates and distribution of molecular hydrogen (H2) in mid-latitude coastal waters". Marine Chemistry 105 (1–2): 129–139. doi:10.1016/j.marchem.2007.01.009. ISSN 0304-4203. 
  16. ↑ "Gas exchange in the filamentous cyanobacterium Nostoc punctiforme strain ATCC 29133 and Its hydrogenase-deficient mutant strain NHM5". Applied and Environmental Microbiology 70 (4): 2137–45. April 2004. doi:10.1128/aem.70.4.2137-2145.2004. PMID 15066806. Bibcode: 2004ApEnM..70.2137L. 
  17. ↑ "Hydrogen production by Trichodesmium erythraeum Cyanothece sp. and Crocosphaera watsonii". Aquatic Microbial Ecology 59: 197–206. 2010-04-08. doi:10.3354/ame01407. 
  18. ↑ "Microbially Mediated Hydrogen Cycling in Deep-Sea Hydrothermal Vents". Frontiers in Microbiology 9: 2873. 2018-11-23. doi:10.3389/fmicb.2018.02873. PMID 30532749. 
  19. ↑ "Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria". Proceedings of the National Academy of Sciences of the United States of America 110 (1): 330–5. January 2013. doi:10.1073/pnas.1215340110. PMID 23263870. Bibcode: 2013PNAS..110..330A. 
  20. ↑ "Hydrogen is an energy source for hydrothermal vent symbioses". Nature 476 (7359): 176–180. 2011-08-10. doi:10.1038/nature10325. PMID 21833083. Bibcode: 2011Natur.476..176P. 
  21. ↑ Jugder, Bat-Erdene; Welch, Jeffrey; Aguey-Zinsou, Kondo-Francois; Marquis, Christopher P. (2013). "Fundamentals and electrochemical applications of [Ni–Fe]-uptake hydrogenases". RSC Advances 3 (22): 8142. doi:10.1039/c3ra22668a. ISSN 2046-2069. 
  22. ↑ Conrad, Ralf; Seiler, Wolfgang (11 July 1988). "Methane and hydrogen in seawater (Atlantic Ocean)". Deep Sea Research Part A. Oceanographic Research Papers 35 (12): 1903–1917. doi:10.1016/0198-0149(88)90116-1. Bibcode: 1988DSRA...35.1903C. 
  23. ↑ Nishihara, Hirofumi; Igarashi, Yasuo; Kodama, Tohru (1989-06-01). "Isolation of an obligately chemolithoautotrophic, halophilic and aerobic hydrogen-oxidizing bacterium from marine environment". Archives of Microbiology 152 (1): 39–43. doi:10.1007/BF00447009. ISSN 1432-072X. 
  24. ↑ Nishihara, Hirofumi; Igabashi, Yasuo; Kodama, Tohruy (1991). "Hydrogenovibrio marinus gen. nov., sp. nov., a Marine Obligately Chemolithoautotrophic Hydrogen-Oxidizing Bacterium". International Journal of Systematic and Evolutionary Microbiology 41 (1): 130–133. doi:10.1099/00207713-41-1-130. ISSN 1466-5026. 
  25. ↑ Vésteinsdòttir H (2008). Physiological and phylogenetic studies of thermophilic, hydrogen and sulfur oxidizing bacteria isolated from Icelandic geothermal areas (PDF) (Masters of Science thesis). University of Akureyri.
  26. ↑ "Physiology and biochemistry of aerobic hydrogen-oxidizing bacteria". Annual Review of Microbiology 35 (1): 405–52. 1981-10-01. doi:10.1146/annurev.mi.35.100181.002201. PMID 6271040. 
  27. ↑ "Hydrogen metabolism in aerobic hydrogen-oxidizing bacteria". Biochimie 60 (3): 297–305. 1978-06-13. doi:10.1016/S0300-9084(78)80826-8. PMID 667183. http://nbn-resolving.de/urn:nbn:de:bsz:352-opus-62888. 
  28. ↑ Appel, Jens; Schulz, Rüdiger (1998-11-01). "Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising?". Journal of Photochemistry and Photobiology B: Biology 47 (1): 1–11. doi:10.1016/S1011-1344(98)00179-1. ISSN 1011-1344. 
  29. ↑ "Localization and stability of hydrogenases from aerobic hydrogen bacteria". Archives of Microbiology 112 (3): 229–38. April 1977. doi:10.1007/BF00413086. PMID 871226. 
  30. ↑ "Regulatory Phenomena in the Metabolism of Knallgasbacteria". Advances in Microbial Physiology. 7. London: Academic Press. 1972. pp. 205–242. doi:10.1016/s0065-2911(08)60079-x. ISBN 9780120277070. 
  31. ↑ Madigan, Michael T.; Martinko, John M; Parker, Jack; Brock, Thomas D. (2003). Brock, biology of microorganisms (10th ed.). Upper Saddle River, N.J: Prentice Hall. ISBN 978-0-13-049147-3. https://archive.org/details/brockbiologyofmi00madi. 
  32. ↑ Yu, Jian; Dow, Allexa; Pingali, Sricanth (2013-07-17). "The energy efficiency of carbon dioxide fixation by a hydrogen-oxidizing bacterium". International Journal of Hydrogen Energy 38 (21): 8683–8690. doi:10.1016/j.ijhydene.2013.04.153. 
  33. ↑ Ishizaki, Ayaaki; Tanaka, Kenji (January 1990). "Batch culture of Alcaligenes eutrophus ATCC 17697T using recycled gas closed circuit culture system". Journal of Fermentation and Bioengineering 69 (3): 170–174. doi:10.1016/0922-338X(90)90041-T. 
  34. ↑ "Solar Foods (Company Website)". https://solarfoods.fi/. 
  35. ↑ Sillman, Jani; Nygren, Lauri; Kahiluoto, Helena; Ruuskanen, Vesa; Tamminen, Anu; Bajamundi, Cyril; Nappa, Marja; Wuokko, Mikko et al. (2019-09-01). "Bacterial protein for food and feed generated via renewable energy and direct air capture of CO2: Can it reduce land and water use?" (in en). Global Food Security 22: 25–32. doi:10.1016/j.gfs.2019.09.007. ISSN 2211-9124. 




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