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Correction ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Microbiol. | doi: 10.3389/fmicb.2019.01959

Corrigendum: Low energy subsurface environments as extraterrestrial analogs

  • 1Bigelow Laboratory For Ocean Sciences, United States

In the original article, there was a mistake in the calculations in Supplementary Table 1 as published, which affected Figure 4 and the resulting text describing Figure 4. In brief, there were errors in the equations for calculating the volumetric energy densities for some of the reactions, due to a copy/paste error, which affected the estimates of cumulative energy density and ratio of reactions presented in Figure 4. We have corrected these errors in the revised Supplemental Table 1 file as well as in Figure 4, shown below. While this is a very regrettable mistake on our part, thankfully the overall message of the article has not changed. We highlight that the error was brought to our attention from a reader who noticed a discrepancy in our Supplemental Data file, emphasizing that peer review works in the end when all data are made available! Published Figure 4. Cumulative volumetric energy densities of redox reactions per site based on environmental concentrations of variables in each reaction (Table 1). Left panel shows the percent contribution of various reactions as shown in the color legend. Right panel shows combined absolute energy density (as kJ per liter) for all reactions, with grey scale reflecting habitat type. All calculations assumed that the electron donor was the limiting substrate. See Supplemental Table S1 for all values and formulas. In the original article, there was an error. A change in the figures required a change in the text. Table 1). For example, on Mars the most energy dense reactions are predicted to be from the NH3/O2, NH3/SO4 2-, and CH4/NO3 -pairs, and all the reactions together are predicted to yield ~10 3 kJ per liter. This overall energy density is similar to the energy density predicted for Titan, although only the NH3/SO4 2-pair would provide energy. The predicted 10 3 kJ per liter energy density in these extraterrestrial targets is also similar at the Juan de Fuca Ridge flank subsurface and in the Rio Tinto ore deposits. Of the Earth subsurface analog sites, the site with the lowest predicted energy density is the anoxic, cold seep brine habitat (roughly 10 milliJoules per liter, mostly from the H2/SO4 2-pair), due to the known absence of most electron acceptors. Likewise, the low predicted energy density for the North Pond cool, oxic basaltic site is due to limited dissolved electron donors. The extraterrestrial site with the lowest predicted energy density is Enceladus (i.e. 1 kJ per liter at the base of the liquid crust interface), which comes almost exclusively from the H2/CO2 couple. This is similar to Lake Vida, which, as an anoxic, ice-environments as extraterrestrial analogs Rose Jones encased hypersaline lake, is a potential analog for proposed conditions on the icy moon. If dissolved oxygen is present in Europa's icy ocean (Teolis et al., 2017), then oxygen reducing reactions would yield the most energy; alternatively, if oxygen is not present, then H2/NO3 and NH4/SO4 may be more dominant. Overall, although based on poorly constrained concentrations, these projections indicate that extraterrestrial sites could have sufficient overall energy to host chemolithotrophic communities.Strikingly, extraterrestrial sites are predicted to have similar cumulative energy densities as Earth's subsurface habitats (with conservative assumptions about electron donor and acceptor concentrations), although the dominant energy-rich processes vary (Figure 4, Supplemental Table 1). For example, cumulative volumetric energy densities on Mars are estimated to range from 0.03-3 kJ L -1 , supported primarily by the electron donors NH3, H2S, or hydrogen reacting with sulfate, nitrate, or oxygen, depending on the scenario chosen for electron donor concentration, pH and temperature. Under the scenario of low electron donor concentration, low pH, and low temperature, the predicted Martian energy density and dominant reactions are similar to those observed at the Earth analog site at the Juan de Fuca Ridge flank subsurface oceanic crust. Under the scenario of higher electron donor concentrations, pH, and temperature, the cumulative volumetric energy density and dominant reactions estimate is more similar to what is estimated from the Earth analog sites in the Rio Tinto. The base of the presumed Europan ocean has an estimated energy density of 400 kJ L -1 fueled primarily by iron oxidation, if dissolved oxygen is present (Teolis et al., 2017) and penetrates to the water-rock interface and if iron is released from water-rock reactions. This volumetric energy density and dominant reaction pattern is similar to that estimated for the Earth analog site at University Valley. By contrast, the ocean on Enceladus is estimated to have an energy density of 100 kJ L -1 fueled by ammonia oxidation with nitrate; none of our comparison Earth analog sites had similar energy density estimates from this reaction. The cumulative volumetric energy density estimates for Titan are the highest we estimate in this exercise, fueled by ammonia oxidation with sulfate or nitrate in a similar pattern as estimated for the Juan de Fuca analog system, but we highlight that this is the least well constrained system. Overall, although based on poorly constrained concentrations, these projections indicate that extraterrestrial sites could have sufficient overall energy to host chemolithotrophic communities.The predicted relative contribution of each redox pair to each site is applicable information for the "follow the energy" approach to habitability (Hoehler, 2007), and can further be constrained by comparison studies of microbial metabolic processes in the Earth analog systems, to see if the predicted energy rich metabolisms are indeed those that occur. This approach of comparing Jones1 et al.Rose Jones energy density to microbial community function has recently been shown for some subsurface sites (Momper et al., 2017;Osburn et al., 2014;Reveillaud et al., 2016), demonstrating the power of this energy density approach to be a useful predictor of metabolic function. For example, North Pond energy is primarily from the FeS2/O2 couple (Figure 4), indicating that solid mineral substrates may be significant in this environment. Information on metabolic function in the community indicates that sulfur oxidizers are present in greater relative abundance as compared to hydrogen, ammonia and nitrite metabolisms (Jørgensen and Zhao, 2016;Meyer et al., 2016), all of which are indicated as possible though with low energy density (Supplementary Table 1). Lost City estimates show ammonia/sulfate as a significant source of energy, tallying with recent work pointing to sulfate metabolisms as being more important than hydrogen metabolisms in this environment (Lang et al., 2018). At this site, the Gibbs free energy of the H2/CO2 couple is relatively high but the energy density low (Figures 3, 4), as dissolved CO2 concentration is scarce because it rapidly precipitates as carbonates in the high pH environment. As shown previously, sulfide oxidizing metabolisms are energy rich in the continental subsurface at the Sanford Underground Research Facility, and sulfide oxidizers are dominant in the microbial community (Momper et al., 2017;Osburn et al., 2014). In the subsurface portion of Rio Tinto, observation of iron and sulfur metabolisms matches with estimates of energy density, although the high energy predicted from the CH4/NO3 couple has not been observed as a dominant metabolism García-Moyano et al., 2012;Sánchez-Andrea et al., 2012) suggesting that other factors may be influencing community structure at this site. Likewise, factors like water availability may be more important than energy availability in structuring the microbial community at the hyperarid and polar desert environments (Goordial et al., 2016). It is notable that the range of conditions at these sites did not particularly affect the volumetric energy density at the hyper-arid sites, unlike the Mars sites, which notably changed. Overall, this "follow the energy" approach of matching predicting energy density to microbial community structure and function may inform the likely metabolisms that might be found on extraterrestrial targets.The predicted relative contribution of each redox pair to each site is applicable information for the "follow the energy" approach to habitability (Hoehler, 2007), and can further be constrained by comparison studies of microbial metabolic processes in the Earth analog systems, to see if the predicted energy rich metabolisms are indeed those that occur. This approach of comparing energy density to microbial community function has recently been shown for some subsurface sites (Momper et al., 2017;Osburn et al., 2014;Reveillaud et al., 2016), demonstrating the power of this energy density approach to be a useful predictor of metabolic function. For example, North Pond energy is primarily from the FeS2/O2 couple (Figure 4), indicating that solid mineral substrates may be significant in this environment. Oxidation of hydrogen sulfide is also predicted to yield more energy than other electron donors (Figure 4), which agrees well with information environments as extraterrestrial analogsRose Jones on metabolic function in the community indicating that sulfur oxidizers are present in greater relative abundance as compared to hydrogen, ammonia and nitrite metabolisms (Jørgensen and Zhao, 2016;Meyer et al., 2016). Lost City estimates show methane and hydrogen oxidation reactions as significant sources of energy (Figure 4), which agrees with work indicating methane oxidizers are common in this system but contrasts with other recent work pointing to sulfate metabolisms as being more important than hydrogen metabolisms in this environment (Lang et al., 2018). At this site, the Gibbs free energy of the H2/CO2 couple is relatively high but the energy density low (Figures 3, 4), as dissolved CO2 concentration is scarce because it rapidly precipitates as carbonates in the high pH environment. As shown previously, sulfide oxidizing metabolisms are energy rich in the continental subsurface at the Sanford Underground Research Facility, and sulfide oxidizers are dominant in the microbial community (Momper et al., 2017;Osburn et al., 2014). In the subsurface portion of Rio Tinto, observation of iron and sulfur metabolisms matches with estimates of energy density García-Moyano et al., 2012;Sánchez-Andrea et al., 2012). The Atacama analog site has a very low predicted energy availability, although we note that factors like water availability may be more important than energy availability in structuring the microbial community at the hyperarid and polar desert environments (Goordial et al., 2016). It is notable that the range of pH and temperature scenarios at the Atacama and University Valley sites did not particularly affect the predicted dominant reactions or volumetric energy densities at the hyper-arid sites, unlike the Mars sites, which notably changed, highlighting that the ion concentrations are key for determining dominant reactions and energy densities. Overall, this "follow the energy" approach of matching predicting energy density to microbial community structure and function may inform the likely metabolisms that might be found on extraterrestrial targets.

Keywords: deep biosphere, subsurface, Astrobiology, Low energy, energy limitation

Received: 07 Aug 2019; Accepted: 08 Aug 2019.

Edited by:

Frontiers I. Microbiology Editorial Office, Frontiers Media SA, Switzerland

Copyright: © 2019 Jones, Goordial and Orcutt. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Beth N. Orcutt, Bigelow Laboratory For Ocean Sciences, Boothbay, Maine, United States, borcutt@bigelow.org