2nd International Planetary Caves Conference (2015 ) 9039 · suggested for the subsurface of Mars [1, 7-9] and no-tionally included in the recent reassessment of Special Regions on

HYPOTHETICAL INVERTED CRITICAL ZONES FOR SUBSURFACE BIOSPHERES ON DESERT PLANETS AND ICY OCEAN WORLDS. P. J. Boston, 1,2. 1Earth & Environmental Science Dept., New Mexico Institute of Mining & Technology, Socorro, NM 87801, [email protected]; 2National Cave & Karst Research Insti-tute, Carlsbad, NM 88222.

Introduction: On Earth, Conditions in cave interiors are typically radically different from and in many ways more benign than the surface environment [1]. Howev-er, the biggest problem for life in caves on Earth is the limitation on energy which for heterotrophic macro-scopic and microscopic cave organisms is largely de-livered as organic material derived from the highly productive surface biosphere to the subsurface by large scale fluid transport, seepage through the rock fracture network, aerial transport into entrances, or biological importation by organisms that forage on the surface but leave fecal and other remains in caves. However, there are many microorganisms who can make their living without this organic nutrient base by making use of the inorganic chemical energy that is present in re-duced gases (e.g. H2S, CO, CH4, H2 etc.) that can come from geological sources below, and oxidation of min-erals particularly those containing metals like iron or manganese. These sources of energy for microbial life have come to be partly understood and discussed for caves on Earth [1-6]. And such a situation has been suggested for the subsurface of Mars [1, 7-9] and no-tionally included in the recent reassessment of Special Regions on Mars [10].

Planet Types with Exclusively Subsurface Bio-spheres: To date, we know of only one type of bio-sphere, namely our own on Earth. Our type of bio-sphere is driven from the outside in by a significant amount of solar energy because we are within the so-called habitable zone of our Sun [11-12] which is de-fined by whether a type of star and distance of a planet from that star can deliver adequate solar energy to sus-tain a photosynthetically driven biosphere. Thus, the scientific community justifiably continues to spend most of its thinking about life in our Solar System and life on exoplanets based on the assumption that all biospheres should behave in this way [13]. However, perhaps we must reconsider this assumption in light of what we have been learning about the subsurface mi-crobial biosphere of Earth, which is reputed to have a biomass that scales at least as large as that of the sur-face and extends to depths of 5km and perhaps further [14, 15]. If this is true, then Earth has both a top-down energy engine (the sun), and a bottom-up energy en-gine (geologically produced energy sources). We have framed this distinction as a Type 1 Biosphere repre-sented by Earth, and a Type 2 Biosphere that could hypothetically be the case on Mars and ice-covered ocean worlds like Europa, Enceladus, and possibly

others within our Solar System (Figure 1). Such a no-tion could also be extended to some of the new classes of planets that are emerging from exoplanet studies for which we have no representatives within our own sys-tem. Earth as a Hybrid Case: In Earth’s subsurface, a host of still poorly understood microorganisms conduct their affairs in a dark world typically under extreme energy limitation, both organic and inorganic. This is often accompanied by extreme temperatures, pressures, or highly reactive gases. Are these organisms just evo-lution’s “losers” who have retreated to the subsurface because they simply can’t compete for delicious sur-face organics? Or are they part of a subterranean mi-crobial biosphere that has persisted over much of Earth’s history and may even have originated there [3,16]? If the latter notion of a permanent indigenous subsurface biosphere is correct, then this suggests an inversion of the ecological concept of a “critical zone” as it is usually applied to surface systems. The concept of critical zone encompasses the lower atmosphere (troposphere and possibly lower stratosphere), the oceans, the continental and island land surfaces, and some depth below the crust that is affected by life and life-derived geochemical and physical processes [17]. The picture that is emerging is that Earth is really a hybrid of a Type 1 and Type 2 Biosphere, but that this has been obscured by the fact that we are surface-inhabiting creatures and are learning about nature be-ginning with what we know and where we live on the surface. Of course, our ignorance about our biosphere and planet is not confined to the terrestrial subsurface but notably applies to the deep oceans and the subsur-face of the ocean crust as well [18]. Microbial Diversity Sweet Spots? Studies of natural caves, both shallow (a few meters) and deep (>1-2 km), and in mines (some >4 km deep) are providing data about the nutritional and evolutionary status of subsurface microbiota although the database so far is very sparse. Although subsurface microbial environ-ments are frequently lumped together, they span a tre-mendous range of different environmental conditions, just as surface habitats do. Are there systematic differ-ences in microbial biodiversity, nutritional strategy, and other properties with depth that may be distin-guishable between shallow, mid-range, and deep crus-tal levels? While it is still early days, predictions can be made and tested as we continue to explore the

9039.pdf2nd International Planetary Caves Conference (2015)

depths. We are predicting for the Earth case, that a decreasing tendency to heterotrophy and an increasing tendency to chemoautotrophy (use of inorganic energy sources) with depth. This is likely to be accompanied by a depth-dependent decrease in total biodiversity as a result of increasing temperatures resulting from the geothermal gradient, spatial restrictions with only tiny rock fracture spaces available at great depth, but in-creasing niche richness with increasing macroporosity (aka “caves”!), and limitations in transport mecha-nisms to move nutrients through the system. We antic-ipate a biodiversity “sweet spot” where heterotrophic and chemotrophic metabolisms optimally overlap (Figure 2). Conclusions: Our biosphere type is only one of sever-al. Caves and the greater subsurface biosphere on Earth can inform us about potential subsurface bio-spheres on desert planets or icy ocean worlds that can be thought of as planet-scale water-filled caves in ice bedrock.

References: [1] Boston P.J. et al (2001) Astrobio 1:25-55. [2] Boston, P.J. et al (2006). Karst Geomorph Hydrol Geo-chem GSA Sp P. 404:331-344. [3] Boston P.J. et al (2009) Hypogene Speleogenesis Karst Hydrology of Artesian Ba-sins. Sp P 1:51-57. [4] Northup D.E. & Lavoie K.H. (2001) Geomicro J 18:199–222. [5] Barton H.A. & Northup D.E. (2007) J Cave Karst Stud 69:163-178 [6] Summers Engel A. (2007) J Cave Karst Stud 69(1):187–206. [7] Boston P.J. et al (1992) Icarus 95:300-308. [8] Fisk M.R. & Giovannoni S.J. (1999) J Geophys Res 104:11805–11815. [9] Le´veille´ R.J. & Datta S. (2010) Planet Space Sci 58:592–598. [10] Rummel J.D. et al (2014). Astrobiol 14(11):887-968. [11] Dole S. (1964) Habitable Planets for Man p. 103. [12] Kasting J. F. et al (1993) Icarus 101(1):108–118. [13] NRC Space Studies Board (2007) Limits Organic Life Planet Syst. [14] Szewzyk U et al (1994) Proc Nat Acad Sci USA 91(5):1810–1813. [15] Takamia H. et al (1997) FEMS Microbiol Lett 152(2):279-285. [16] Summers-Engel A. & Northup D.E. (2008) KWI Sp P 37-48. [17] National Re-search Council (2001) Basic Res Opportun Earth Sci. [18] Santelli C.M. et al (2008) Nature 453:653-656.

What Kind of Planet Biosphere Is It?

Planet Type 1 Biosphere Sunlight “just right” for photosynthesis Green Gooey Gases in non-equilibrium Critical Zone is top-down Photosynthetically driven

Planet Type 2 Biosphere No visible means of support on surface Not green (or other photosynthetic pigment) Not gooey! Atmospheric gases in chemical equilibrium (Exceptions dependent upon crustal leakiness) Critical Zone is bottom-up Chemosynthetically driven

Well mixed-Critical Zone Stratified Critical Zone

Mixing between oceans, atmosphere, crust, and biosphere.!

Mixing between subsurface compartments only. Roofed by bedrock or ices.!

Figure 1: Contrast between the two major hypo-thetical categories of Biospheres that we may expect to encounter on inhabited planets, both within our Solar System and in other systems.

Figure 2: Notional biodiversity sweet spot in Earth’s subsurface representing an overlap in nutrient and enenrgy sources derived from above (organics) and below (geo-gases and mineral energy sources).

9039.pdf2nd International Planetary Caves Conference (2015)