By Jessica Kowalik, George Washington University
From deep-sea hydrothermal vents to our own gastrointestinal biomes, bacteria that convert hydrogen to energy are a crucial and fascinating component of microbial ecosystems. Their hydrogen consumption may hold the key to explaining why certain animals are able to flourish several kilometers beneath the sea and how human pathogens can survive in our gastrointestinal tracts to cause disease and, potentially, even cancers.
When most people think of hydrogen as an energy source, they probably picture biofuel production for sustainable energy; but bacteria have beaten us to it, using hydrogen to satisfy their own energy needs. Deep-sea hydrothermal vents, first discovered in 1977, contain mollusks coated by fluids replete with hydrogen and an internal symbiotic population of bacteria that consume hydrogen. Such bacteria are formally included in the category of lithotrophs, also called autotrophs, organisms that use carbon dioxide as a carbon source and utilize inorganic materials such as hydrogen for energy. Thanks to hydrothermal vents, hydrogen has become the first chemical energy source of symbiotic relationships between animals and microorganisms to be discovered in 25 years, a discovery that carries critical implications for our internal ecosystem as well.
Hydrothermal vents offer a mine of energy: fluids coursing through the vents carry compounds rich in electrons and these are transported like the current in a battery. Wildlife on the ocean floor use the energy to build an ecosystem in this seemingly inhospitable environment. Most fauna on the ocean floor, however, lack oral cavities or the internal metabolic means to utilize the energy flow, requiring symbiotic microbes to play a crucial role. Though the bacteria do not literally breathe in hydrogen, they ingest it to generate energy for themselves and their sea floor hosts. Hydrogen in this environment is abundant from reactions between seawater and crustal rocks.
Peterson et al. determined that bacteria using the previously known energy sources in hydrothermal vents, hydrogen sulfide and methane, are also capable of consuming hydrogen. They observed that bacteria inside mussels fixed carbon dioxide by using hydrogen as an electron donor for an energy source at a rate comparable to using methane or sulfide for energy. The team further discovered a critical gene, hupL, which encodes a portion of hydrogenase, the enzyme that allows for oxidation of hydrogen. The gene is found on a Bathymodiolus mussel DNA fragment that includes the genes necessary for oxidation of sulfide. DNA of the tubeworm Riftia pachyptila and of the shrimp Rimicaris exoculata also contains hupL. While certain microbes only synthesize hydrogenase if exposed to hydrogen, others always maintain the enzyme in low levels that increase if more hydrogen is available. Regardless, hydrogen utilization has been observed to increase when these bacteria are exposed to higher levels of hydrogen.
Why use hydrogen?
The selection of hydrogen for energy use at first appears extraordinary considering the availability of many other possible fuel sources including ammonium, ferrous iron, and manganese (II), all of which are utilized by other documented vent microorganisms. This phenomenon may be explained by the high energy yield derived from hydrogen as opposed to other sources. For example, aerobic hydrogen respiration in the hydrogen-rich Logatchev vent field can produce as much as seven times more energy per kilogram of fluid than methane oxidation and 18 times more energy than sulfide oxidation.
To date, the highest concentration of hydrogen discovered in a hydrothermal vent is located in the Logatchev vent field on the Mid-Atlantic Ridge (Figure 1). Bathymodiolus puteoserpentis mussels are the most prolific of the macrofauna in Logatchev, host to sulfide and methane oxidizers in their gills.
Hydrogen uptake by bacteria is not limited to vents abounding with hydrogen, however. For instance, Comfortless Cove and Lilliput, vent fields on the southern Mid-Atlantic Ridge, are significantly lower in hydrogen concentration than Logatchev. Peterson et al. illustrated that in spite of lower hydrogen levels, Bathymodiolus mussel species were still capable of hydrogen intake, albeit at rates 20 to 30 times less than those recorded by Logatchev mussels. Yet, when gill tissues from each vent site were exposed to more hydrogen, all increased hydrogen ingestion; hence, as previously discussed, higher hydrogen concentrations correlate with great consumption.
Where are they usually found?
Given the prevalence of animal-microbe symbiotic relationships like those within Bathymodiolus puteoserpentis, other such symbioses are expected to be found in the near future. Peterson et al. uncovered indications of a symbiotic relationship in Rimicaris exoculata shrimp in hydrothermal vents that may also utilize hydrogen for energy.
On average, hydrothermal vents are located two kilometers deep or more below the ocean surface. Due to the depth and highly volatile physical and chemical conditions of vents, scientists have only been able to obtain samples using submersibles, which transport researchers to the ocean floor, and robots operated remotely. Though the majority of hydrogen bacteria research has focused on deep-sea vents given recent discoveries, hydrogen may also be an energy source for bacteria with immediate effects on the human population.
Why should we care?
The knowledge that some bacteria employ hydrogen to produce energy is only the beginning of the story. Most importantly for humans, hydrogen bacteria may have significant health implications. Like seabed fauna, we too have an entire ecosystem of bacteria within our bodies but, unlike vent mollusks, we do not have a symbiotic relationship with the hydrogen bacteria present in our system. Hydrogen appears to be a virulence factor for the pathogenic bacteria Helicobacter pylori, which causes gastritis and peptic ulcers and has been associated with certain kinds of gastric cancers. Hydrogen is excreted in rodent and human gastrointestinal tracts, and scientists have recently established that multiple Helicobacter species, including H. pylori, living in human and animal tracts are able to utilize hydrogen for energy. Particularly since neither humans nor animals can use this hydrogen, it provides an energy supply to pathogens living in low-energy environments like our gastrointestinal mucous membranes (Figure 2). Given that it remains uncertain which energy sources are used by pathogens after invading their host, hydrogen use may prove an invaluable means of understanding how certain pathogens flourish inside their human hosts. With greater understanding of these mechanisms, we will be better equipped to combat pathogens responsible for human diseases, some of which are related to cancers.
Future research needs to investigate which microbes consume hydrogen and to what degree. Additionally, their biology and environment must be considered more to fully understand when and how frequently hydrogen is used in their respective ecosystems, particularly that most extraordinary microscopic ecosystem of all: the human body.
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