Chemotrophy Along Seafloor Hydrothermal Vents

From MicrobeWiki, the student-edited microbiology resource

by Pamela Moriarty


Life Along the Hydrothermal Vents

Earth’s oceans are populated by microorganisms which perform a wide range of important services. Three oceans, the Atlantic, Pacific and Indian, contain hydrothermal vents along their floor. Hydrothermal vents are formed where ocean plates pull apart and hot, mineral rich water and lava escape. Living along or in hydrothermal vents can pose great challenges to microorganisms. Most deep-sea hydrothermal vents contain low amounts of Mg2+, SO42-, and total S, while being abundant in silica, metals and dissolved gases. Seawater circulation allows for ion exchange and helps carry certain molecules, such as NH4+, Fe2+, Mn2+, H2S, H2, CO, and CH4, to the deep sea. However, this leads to more challenges for microorganisms inhabiting the vents, as the high concentrations of Fe2+, and NH4+ can affect metabolism (Karl 1995). The high pressure along the entire sea floor also presents challenges. Finally, temperature is extremely variable, supporting both psychrophiles living below 10⁰C and superthermophiles living above 115⁰C (Van Dover 2000). The wide range of environments occurring by the hydrothermal vents on the ocean floor present a set of unique challenges to microorganisms. We are just beginning to understand the variety of adaptations they have evolved to meet these challenges. While some environmental conditions remain the same from vent to vent, there are also major differences between vents in potential carbon and energy sources available . In addition, there are nutrient gradients within vent ecosystems due to circulation patterns. Each vent typically contains four distinct microbial habitats: 1) emitted vent fluid that contain free-living microbial populations, 2) rock, chimney, sediment and animal surfaces exposed to vent fluids that contain free-living microbial populations, 3) vent fauna and microorganisms in endo and exosymbiotic relationships and 4) the hydrothermal vent plumes. (Karl 1995).

The metabolic processes used by microorganisms in these environments span a wide range of electron donors and acceptors. Many, if not most, microbes along the hydrothermal vents practice mixotrophy, using combinations of different metabolic pathways based on what is available in the highest concentrations. Potential aerobic chemosynthetic processes include oxidation of sulfur compounds including sulfide, thiosulfate, hydrogen sulfide and elemental sulfur, as well as iron, manganese, carbon-compound and hydrogen oxidation and nitrification, while anaerobic chemosynthetic possibilities include sulfur or sulfate reduction, denitrification and methanogenesis. In the environment, aerobic chemosynthesis uses O2 as the electron acceptor, which has relatively large energy yields, allowing for the production of large amounts of biomass. Under anaerobic conditions, H2 is typically the electron donor. Hydrogen oxidation also yields high amounts of energy, but along the hydrothermal vents the low amounts of hydrogen available mean that little biomass can be produced through anaerobic chemosynthesis. Most likely, sulfide oxidation accounts for most of the energy available in this environment. (Van Dover 2000).

In addition to chemotrophy, two alternative hypotheses of energy production have been proposed. The first is organic thermogenesis, in which organic simple molecules such as thiocyanate and glycine are generated abiotically when sea water and hot rock react at large depths. Some sulfur compounds can also be synthesized from formaldehyde and sulfur that are in hydrothermal vent fluids. Other organic thermogenesis pathways include the possibility of producing urea, alkanes and alkenes abiotically. Another proposed hypothesis is detrital thermal alteration, which occurs when refractory organic carbon is thermally degraded to petroleum hydrocarbons and volatile fatty acids, which can be used by heterotrophic microbes. While these have not been extensively studied, they are interesting alternatives for energy production. (Van Dover 2000).

Microorganisms inhabiting hydrothermal vents have many possible biotechnological applications. One possibility is using microbes for bioremediation of waste sulfides and returning the resulting sulfate to the oceans and using the bacterial biomass as food for aquaculture or fermenting it into synfuels. Hyperthermophilic bacteria may also provide enzymes useful in a variety of molecular techniques including PCR, amylases, glucosidases and proteases as they are stable at a wide range of temperatures and may also be resistant to detergents and organic solvents. (Van Dover 2000).

It was long thought that there was no life along deep-sea hydrothermal vents because organisms would not be able to produce enough energy to live. Obviously this is now known to be incorrect, as microbes there have been found to be diverse and abundant, and larger organisms, including mussels, snails, sponges and shrimp have been found, though there are likely thousands more microorganisms that are unculturable that we have not yet discovered or been able to identify. Oxidation and reduction of sulfur are thought to be the prevalent metabolic pathways for life along the hydrothermal vents. Methylotrophy and methanogenesis also play extremely important roles, while iron, manganese, hydrogen and ammonia oxidation are just beginning to be studied in depth.


Oxidation and Reduction of Sulfur Compounds

Some of the most common pathways of energy production in microorganisms who live along the hydrothermal vents are oxidation or reduction of sulfur compounds. The most common electron donor along the vents is hydrogen sulfide, making oxidation of sulfur containing compounds the base of the food web in this environment (Van Dover 2000, Jannasch 1995). The microorganisms in this environment capable of oxidizing or reducing sulfur compounds show amazing diversity. Over 161 gram-negative sulfur-oxidizing bacteria species have been found to inhabit the hydrothermal vents. Bacteria in this environment are often thought of as all being autotrophs, but of these 161 species, over 97% are also capable of heterotrophic growth. In addition, 37% perform fermentation and 88% perform denitrification (Van Dover 2000). Furthermore, the sulfate reducers known to be present include at least nine different genera, including gram-negative and positive species. While most are rod shaped or vibrios, others are ovoid or filamentous. Some of the microorganisms have been found to only perform partial oxidation of a limited range of carbon sources, while others can perform oxidation with short and long chain fatty acids and organic compounds (Hamilton 1987). The diversity that has already been discovered is astonishing.

S-oxidizing bacteria (those that oxidize sulfur, sulfate, thiosulfate or other sulfur compounds) include chemolithoautotrophs, chemolithoheterotrophs, chemolithomixotrophs and chemoorganoheterotrophs. Most use oxygen as a terminal electron acceptor, though some are capable of using nitrate. Thiosphaera panotropha is even capable of using oxygen and nitrate simultaneously (Karl 1995).

S-reducing bacteria can use sulfate, thiosulfate, or elemental sulfur as their terminal electron acceptor. The byproduct is typically sulfide. S-reduction produces a much lower amount of energy than reducing oxygen or nitrogen. If one mole of lactate is oxidized with oxygen as the electron acceptor 298 kcal is released, while if sulfate is the electron acceptor, just 9.7 kcal is released. However, the abundance of sulfate along the hydrothermal vents makes this a profitable metabolic pathway for many microorganisms.

Gsb1.JPG

Many microbes, in many different environments, practice mixotrophy. Along the hydrothermal vents microbes commonly perform oxidation or reduction of S-compounds along with other methods to produce more energy. An interesting combination, found by Beatty et al., is performed by a photosynthetic anaerobe that also oxidizes sulfur compounds. The bacteria GSB1 was found in a hydrothermal vent plume in the East Pacific Rise. While geothermal light was known to exist, it was not previously thought to be enough for photosynthesis to occur. However, the discovery of this microbe changes that view. GSB1 is believed to be a green sulfur bacteria. It is rod shaped, gram-negative and contains chlorosomes. When isolated in pure culture it absorbed similar wavelengths to Chlorobium and Prosthecochloris. The peak absorbance occurred at about 750 nm and peak fluorescence occurred at about 775 nm, implying that GSB1 contains bacteriochlorophyll c. GSB1 also absorbed efficiently around 450 nm, indicating the presence of carotenoids. Using mass spectroscopy, the carotenoids were identified to most likely be chlorobactene. The 16S rRNA sequence of GSB1 is similar to that of Chlorobium and Prosthecochloris, however it also has a unique Fenna-Matthews-Olson (FMO) protein to harvest light. The FMO proteins most similar to it are again found in Chlorobium and Prosthecochloris. Due to these similarities, GSB1 was determined to be related to the Chlorobium and Prosthecochloris genera. GSB1 is obligately photosynthetic, requiring light in addition to hydrogen sulfide or elemental sulfur and carbon dioxide to grow. The discovery of an obligate photosynthetic green sulfur bacteria along the hydrothermal vents of the ocean floor is fascinating, and opens the door to the possibility of life in other environments have been thought to be inhabitable. (Beatty et al. 2005)

In addition to mixotrophy, S-oxidizing bacteria are commonly found in symbiotic relationships along the hydrothermal vents. They have been found in at least 5 families of bivalves (Karl 1995), tube worms, and snails. Two meter long tubeworms that contain no mouth or gut have been found. These are able to exist only due to chemoautotrophic endosymbionts. The tubeworm’s trophosome’s was found to be packed with prokaryotic cells that produce organic material from inorganic compounds obtained from the tubeworm. The bacteria then transfer organic material back to the host to allow it to survive. Bathymodiolus mussels, vesicomyid clams and pectinid scallops also have chemoautotrophic bacteria that live in their gills. The gastropod Ifremeria nautilei has 15-20 times the number of gill filaments and a stomach 1/10 of the size of members of its family that do not contain endosymbionts. (Van Dover 2000)

At the Lau Basin hydrothermal vents in the Pacific Ocean, the distribution of two species of snails, Alviniconcha sp. 1 and Infremeria nautilei and a mussel, Bathymodiolus brevior, was found to be in concentric circles around a diffuse hydrothermal source at least partially due to the pattern of reduced sulfur compounds. The Alvinconcha were present in the water with the highest concentration of sulfide. Moving out to the I. nautilei, the concentration of polysulfides increased as the concentration of free sulfide dropped, and among the B. brevior thiosulfates were prevalent, with free sulfide concentrations sometimes undetectable. All 3 organisms depend on endosymbionts to produce energy and the variation in the species of symbionts they contain results in different preferences for types of sulfur compounds. The pattern of concentric circles allows each microbe species maximum exposure to their preferred sulfur source, thereby allowing the larger organism to obtain maximum energy. (Waite et al. 2008)

Methylotrophy and Methanogenesis

Include some current research in each topic, with at least one figure showing data.


Less Common Pathways- Iron, Manganese, Hydrogen and Ammonia Oxidation

Include some current research in each topic, with at least one figure showing data.


Conclusion

Overall paper length should be 3,000 words, with at least 3 figures.


References

Beatty, Thomas J., Jorg Overmann, Michael T. Lince, Ann K. Manske, Andrew S. Lang, Robert E. Blankenship, Cindy L. Van Dover, Tracey A. Martinson, F. Gerald Plumley, and Bob B. Buchanan. “An Obligately Photosynthetic Bacterial Anaerobe from a Deep-Sea Hydrothermal Vent.” Proceedings of the National Academy of Sciences of the United States of America. 2005. Volume 102. p. 9306-9310.

Dick, Gregory J., Yifan E. Lee and Bradley M. Tebo. “Manganese (II)-Oxidizing Bacillus Spores in Guaymas Basin Hydrothermal Sediments and Plume.” Applied and Environmental Microbiology. 2006. Volume 72. p. 3184-3190.

Duperron, Sébastien, Claudi Bergnin, Frank Zielinski, Anna Blazejak, Annelie Pernthaler, Zoe P. McKiness, Eric DeChaine, Colleen M. Cavanaugh and Nicole Dubilier. “A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge.” Environmental Microbiology. 2006. Volume 8. p. 1441-1447.

Hamilton, W. Allan. “Sulphate-reducing Bacteria and the mechanism of corrosion in the marine environment.” 1987. In: Microbes in the Sea, ed. Michael A. Sleigh. Ellis Horwood Limited, England, p. 190-202.

Karl, David M. “Ecology of Free-Living, Hydrothermal Vent Microbial Communities.” 1995. In The Microbiology of Deep-Sea Hydrothermal Vents, ed. David M. Karl. CRC Press, Boca Raton, p. 35-124.

Jannasch, Holger W. “Microbial Interactions With Hydrothermal Fluids.” 1995. In: Seafloor Hydrothermal Systems- Physical, Chemical, Biological and Geological Interactions, ed. Susan E. Humphris, Robert A. Zierenberg, Lauren S. Mullieneaux and Richard E. Thomson. American Geophysical Union, United States, p. 273-296.

Johnson, Eric F. and Biswarup Mukhopadhyay. “A New Type of Sulfite Reducatase, a Novel Coenzyme F420-dependent Enzyme, afrom the Methanarchaeon Methanocaldococcus jannaschii.” The Journal of Biological Chemistry. 2005. Volume 280. p. 38776-38786.

Satoshi, Nakagawa and Ken Takai. “Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance.” FEMS Microbiology Ecology. 2009. Volume 65. p. 1-14.

Sherr, Evelyn and Barry Sherr. “Marine Microbes: An Overview.” 2000. In: Microbial Ecology of the Oceans, ed. David L. Kirchman. Wiley-Liss, Inc, New York, p. 13-46.

Schmidt, Caroline, Renaud Vuillemin, Christian Le Gall, Françoise Gaill and Nadine Le Bris. “Geochemical energy sources for microbial primary production in the environment of hydrothermal vent shrimps.” Marine Chemistry. 2008. Volume 108. p. 18-31

Teske, Andreas, Ashita Dhillon, and Mitchell L. Sogin. “Genomic Markers of Ancient Anaerobic Microbial Pathways: Sulfate Reduction, Methanogenesis and Methane Oxidation.” Biological Bulletin. 2003. Volume 204. p. 186-191.

Van Dover, Cindy Lee. The Ecology of Deep-Sea Hydrothermal Vents. 2000. Princeton University Press, Princeton, 424 p.

Waite, Tim J., Tommy S. Moore, James J. Childress, Helen Hsu-Kim, Katherine M. Mullaugh, Donald B. Nuzzio, Amber N. Paschal, Jeffrey Tsang, Charles R. Fisher, and George W. Luther III. “Variation in Sulfur Speciation with Shellfish Presence At a Lau Basin Diffuse Flow Vent Site.” Journal of Shellfish Research. 2008. Volume 27. p. 163-168.


Edited by student of Joan Slonczewski for BIOL 238 Microbiology, 2009, Kenyon College.

Retrieved from "http://microbewiki.kenyon.edu/index.php/BIOL_238_Paper_2009"