Contradistinction to the Klingler hypothesis

Model estimates indicate that impacts, hydrodynamic escape and sputtering removed 99% of the Mars's initial atmosphere (McElroy et al. Reference McElroy, Kong and Yung1977; Bogard et al. Reference Bogard, Clayton, Marti, Owen and Turner2001). Earth scaling and models estimated an initial nitrogen atmospheric inventory ranging from 2 to 300 mbar (McKay & Stoker Reference McKay and Stoker1989), providing, at most, over three orders of magnitude more nitrogen for a primordial Martian biosphere. Taking into account Mars' current atmospheric nitrogen content (i.e. 0.2 mbar), this yields a maximum nitrogen missing sink of 2.8 mbar (9×10¹⁵ kg of N). A maximum nitrogen missing sink of 2.8 mbar is plausible as atmospheric nitrogen would accumulate over millennial time frames in the near-surface (i.e. top few metres) as water infiltration and leaching are minimal (Walvoord et al. Reference Walvoord2003; Graham et al. Reference Graham, Hirmas, Wood and Amrhein2008). Were the current entire atmospheric reservoir to be converted into biomass, Mars could at most support ∼10¹⁵ kg of biomass, or roughly 1 kg m⁻² over the surface. By comparison, primary productivity (photosynthetic) on Earth is ∼10¹⁴ kg yr⁻¹ (Field et al. Reference Field, Behrenfeld, Randerson and Falkowski1998). The terrestrial mass ratio of nitrogen in biomass to that in the atmosphere is ∼10⁻⁵ (Capone et al. Reference Capone, Popa, Flood and Nealson2006); if this ratio were to hold for Mars, we might expect ∼10¹⁰ kg of total biomass. Therefore, micro-organism growth could clearly not be supported if the only nitrogen source were from the atmosphere. However, if the 9×10¹⁵ kg of subsurface N were added to the mix, then biological processes could still be occurring (Klingler et al. Reference Klingler, Mancinelli and White1989). If just 10% of the atmospheric nitrogen lost between early Mars and contemporary Mars went into abiotic or biogenic sediments, from an initial nitrogen inventory of 18 mbar (Fox & Delgarno Reference Fox and Delgarno1983; Klingler et al. Reference Klingler, Mancinelli and White1989), then ∼10¹¹ kg should be expected in the Martian rock record, comparable to the nitrogen sequestered in sediments on Earth, ∼10¹¹ kg (Field et al. Reference Field, Behrenfeld, Randerson and Falkowski1998).

Activity on the Martian surface is limited to diffusion and heterogeneous photochemical processes. Lateral dissolution of atmospheric species would occur in thin liquid films with thicknesses ranging from ∼1 to 6 nm given atomic diameters are ∼1 to a few angstroms. Therefore, lateral dissolution of HNO₃ would occur at Mars' surface. 1D gas-phase photochemical simulations, constrained by Viking NO measurements, made in the upper Martian atmosphere, show that HNO₃ is one of the principal reservoir species for nitrogen in its lower atmosphere, representing ∼10⁻¹¹ of Mars' current total nitrogen content. The Henry's law coefficients of other nitrogen oxides’ are orders of magnitude smaller than HNO₃. For instance, the Henry's law coefficient for N₂, NO, NO₂, N₂O, HNO₂ and HNO₃ are 6×10⁻⁴, 2×10⁻³, 1×10⁻², 3×10⁻², 49 and 2×10⁵ M atm⁻¹, respectively. Therefore, the dissolution of gas-phase HNO₃ is extremely efficient. 1D photochemical simulations show that the current steady-state concentration of HNO₃(g) just above the Martian surface is ∼5×10⁵ molec. cm⁻³ (8×10⁻¹⁶ M of NO₃⁻), which represents ∼10⁻¹¹ % of the total atmospheric nitrogen content, just above the Martian surface. Given that the total amount of thin liquid film ranges from 3.5×10⁶ to 2×10⁷ litres, 2×10⁻⁹ moles (1.5×10⁻¹⁰ kg) to 2×10⁻⁷ moles (1.5×10⁻⁸ kg) of NO₃⁻ is available at the Martian surface. Dissolution of N₂ may also occur on slower timescales as its Henry's law constant is 6×10⁻⁴ M atm⁻¹. The current steady-state concentration of N₂(g) just above the Martian surface is ∼5×10¹⁵ molec. cm⁻³ (9.6×10⁻⁶ M N₂), which equates to ∼10⁻⁶ % of the total atmospheric nitrogen content and ∼30 moles (1 kg) to ∼3000 moles (80 kg) of N₂ (i.e. the amount of N₂ that would be available at the Martian surface). Within these contexts, potential life would have to thrive under conditions of severe nitrogen deficiency as [HNO₃] and [N₂] in the Martian atmosphere is a small fraction of their respective amounts in Earth's atmosphere (e.g. ∼10⁻⁵ to 0.03, respectively, at the surface, Fig. 1).

Fig. 1. 1D model simulation of altitude (km) versus [HNO₃(g)]_Mars/[HNO₃(g)]_Earth and [N₂(g)]_Mars/[N₂(g)]_Earth.

Exothermic reactions as a source of energy for nitrogen fixation

Weiss et al. (Reference Weiss, Yung and Nealson2000) showed that subsurface Martian organisms could be supplied with a large energy flux from the oxidation of photochemically produced atmospheric H₂ and CO diffusing into the regolith. Surface abundance measurements of these gases demonstrate that not more than a few percent of this available flux is actually consumed, suggesting that biological activity driven by H₂ and CO is limited in the top few hundred metres of the subsurface, far exceeding the energy derivable from other atmospheric gases. They show for organisms at 30 m depth that the hydrothermal and chemical weathering energy is 2000 times more than previous estimates. This implies that the apparent scarcity of life on Mars is not attributable to lack of energy. The following thermodynamic calculations support this notion as exothermic reactions may occur on thin liquid films to release energy for nitrogen fixation.

Nitrogen is linked by a very strong triple bond and is energetically expensive (bond strength ∼945 kJ mole⁻¹ – see reactions (1) and (2)). Fixed nitrogen (i.e. NH₃, NH₄⁺ and NO_x or nitrogen that is chemically bound to either inorganic or organic molecules that can be released by hydrolysis to form NH₃ and NH₄⁺) is useful to living organisms (Ducluzeau et al. Reference Ducluzeau, Lis, Duval, Schoepp-Cothenet, Russell and Nitschke2009). Available quantities of free energy are crucial for supporting life and debated in terms of it being a requirement for nitrogen fixation:

(1)

(2)

For chemical reactions, we are often interested in the change in Gibbs free energy (ΔG),

(3)

where P is the pressure, T is the temperature, R is the universal gas constant, Q is the reaction quotient, A, B, C and D are reactants, respectively, m, n, x and y are coefficients of reactants, and products ΔG^o is the standard free energy change (at 1 bar and 25°C). The standard free energies for nitrogen, oxygen, water and nitric acid in the following reaction

(4)

are, respectively 0, 0, −236.65 and −110.88 kJ mole⁻¹, yielding ΔG^o=7.45 kJ mole⁻¹. This reaction, requiring a positive change in Gibbs free energy, is not spontaneous and will proceed only with the addition of energy. We can now calculate conditions when the above reaction will proceed without the addition of free energy. Given Mars's mean atmospheric surface pressure of 5.53×10⁻³ atm (or 5.6 mbar), its N₂(g) and O₂(g) abundances are 2.7% and 0.13%, respectively, we approximate N₂(g) and O₂(g) pressures to be 1.49×10⁻⁴ and 7.19×10⁻⁶ atm, respectively. We assume here that water in the form of thin liquid films had unit activity. So, at equilibrium:

(5)

(6)

(7)

(8)

This value corresponds to a concentration of ∼3 nm (Lide Reference Lide2006). So, as long as [HNO₃(aq.) or NO₃⁻] remains below ∼3 nm, reaction (2) will proceed with the liberation of free energy.

Given the fact that [HNO₃(aq.) or NO₃⁻] is likely smaller than ∼3 nm (e.g. 8×10⁻¹⁶ M of steady-state HNO₃ by 1D photochemical simulations) there is heat (not work) liberated for partial use as chemical energy. The more dilute the concentration at which nitrate is formed, the greater the amount of available work (not heat) will be available. If we assume that [HNO₃] ranges from 10⁻¹⁶ to 10⁻⁹ M and the activity coefficient at this concentration is unity, the following calculations show that the free energy is

(9{\rm a})

(9{\rm b})

Then

(10)

These calculations show that the negative change in Gibbs free energy increases with decreasing HNO₃. In other words, for the low concentration of HNO₃ (in the form of NO₃⁻), we expect for pure water thin liquid films on the surface of Mars, reaction (2) is exergonic and may proceed spontaneously. Figure 2 exemplifies the relationship between the change in Gibbs free energy and HNO₃ concentration. Temperatures shown correspond to the 186, 227 and 268 K. For the warmest temperature, HNO₃ concentrations of <10⁻⁹ M yield a negative change in Gibbs free energy. At 186 K, concentrations of <3×10⁻¹¹ M yield a negative change in Gibbs free energy. At the mean surface temperature of Mars (227 K), an HNO₃ concentration of 8×10⁻¹¹ M or less yields a negative change in Gibbs free energy.

Fig. 2. The change in Gibbs free energy (ΔG) versus HNO₃ concentration at 186, 227 and 268 K.

The foregoing analyses fail to serve for anaerobic organisms, such as Clostridium, which can fix nitrogen in the absence of oxygen. The production of aqueous ammonia from nitrogen and hydrogen is attended by ΔG^o=−26 and ΔH^o=−84.84 kJ mole⁻¹ (reaction 4).

(11)

In comparison, if oxygen were present (reaction 11), replacing water (reaction 11), ΔG^o=−263.01 kJ mole⁻¹.

(12)

An analogous assessment can be made between reactions (2) and (12), where ΔG^o=−110.88 and ΔH^o=−205.44 kJ mole⁻¹ in reaction (12) due to the presence of hydrogen

(13)

Photochemical reactions as a source of energy for nitrogen fixation

Other forms of energy, such as UV radiation at the Martian surface can also produce fixed nitrogen species, such as NO(g) and NO₂(g) via photolysis of HNO₃(g) and NO₃⁻ (aq.), which has been investigated extensively in the lab (Dubowski et al. Reference Dubowski, Colussi, Boxe and Hoffmann2002; Boxe et al. Reference Boxe2003, Reference Boxe2005,  Reference Boxe2006) and to a limited extent via multiphase modelling (Boxe & Saiz-Lopez Reference Boxe and Saiz-Lopez2008). The gas phase concentration of HNO₃ at the surface of Mars is ∼5×10⁵ molec cm⁻³, which is equivalent to 8×10⁻¹⁶ M of NO₃⁻. Since Boxe & Saiz-Lopez (Reference Boxe and Saiz-Lopez2008) calculated a 3×10⁴ concentration enhancement from 9 μM NO₃⁻ in a 300-nm-thick liquid layer, we calculate a 4.5×10⁵ concentration effect for 8×10⁻¹⁶ M of NO₃⁻ absorbed in a 6-nm-thick interfacial film. We then initialize our model with [NO₃⁻]=4×10⁻¹⁰ M. The actinic flux spectrum at the surface of Mars is from 200⩽λ/nm⩽400 (Yung & Demore Reference Yung and Demore1999) so the condensed phase model incorporates the predominant reactions representative of nitrate photochemistry in this wavelength region. The actinic flux spectrum for Mars' was also weighted to take into account NO₃⁻ absorption bands centred at 201 nm (ε_max=9500 M⁻¹ cm⁻¹) and 302 nm (ε_max=7.14 M⁻¹ cm⁻¹) and NO₂⁻ absorption bands centred at 220 nm (ε_max=5800 M⁻¹ cm⁻¹), 318 nm (ε_max=10.90 M⁻¹ cm⁻¹) and 354 nm (ε_max=22.90 M⁻¹ cm⁻¹). A volumetric factor was quantified by taking the average of the upper and lower limit reaction rate enhancement factors (unit-less numbers), obtained in the laboratory by Grannas et al. (Reference Grannas, Shepson and Filley2004) and Takenaka et al. (Reference Takenaka1996), 40 and 2.4×10³, respectively, yielding 1.22×10³. Therefore, the reaction rates are quantified by incorporating a volumetric factor, volumetric. Table 1 lists the major reactions pertaining to nitrate photochemistry, their condensed phase reaction rates and their interfacial reaction rates. Although we scale the secondary and tertiary non-photolytic reaction rates to give a thorough representation of nitrate photochemistry on the Martian surface, as shown by Boxe & Saiz-Lopez (Reference Boxe and Saiz-Lopez2008), the photolytic reactions dominate the evolution of NO, NO₂ and NO₂⁻.

Table 1. Interfacial film reactions and rate constants

^a Aqueous phase reaction rate constants were obtained from Mack & Bolton (Reference Mack and Bolton1999).

^b QLL rate reaction rate constants were quantified by including the ‘volumetric’ factor (Grannas et al. (Reference Grannas, Bausch and Mahanna2007), Takenaka et al. (1996)).

^c values were extrapolated from Qui et al. (Reference Qiu, Green, Honrath, Peterson, Lu and Dziobak2002) and King et al. (Reference King, France, Fisher and Beine2005).

^d was extrapolated from Zuo & Deng (Reference Zuo and Deng1998).

^e Volumetric ∼8.20×10⁻⁴ (Grannas et al. (2007); Takenaka et al. (1996)).

Figure 3 shows a diurnal profile of NO, NO₂ and NO₂⁻ evolution in a 20-nm-thick interfacial film due to heterogeneous photochemical processing of NO₃⁻. NO, NO₂⁻ and NO₂ exhibit maximum concentrations of 1.3×10², 2×10³ and 9.4×10³ molec cm³. Although the total integrated flux over 200–400 nm at the surface of Mars is comparable to the Earth's, the shorter wavelengths contribute a much greater proportion of this UV flux (e.g. 200⩽λ/nm⩽315). This is, the fact that NO₂ is a primary photolytic product, due to its greater branching ratio (compared to NO₂⁻) for photolytic production combined with the fact that NO₃⁻ centred at 201 nm has a greater absorption band, compared to the NO₂⁻ absorption band centred at 220 nm explains the greater production of NO₂, compared to NO. In addition, the decrease in contribution of the actinic flux spectrum at λ>315 nm also helps to explain the smaller amount of NO produced in the thin liquid film since nitrite's absorption bands are centred at 318 and 354 nm. The concentration of NO₃⁻ in the interfacial film is constant due to the small quantum yield for NO₂ and nitrite production and the fact that NO₃⁻ is replenished by atmospheric deposition of HNO₃. This phenomenon implies that Martian surface is not a permanent sink for atmospheric nitrogen (Fig. 3).

Fig. 3. Simulated evolution as a function of time (hours) and concentration molec cm³ of NO, NO₂ and NO₂⁻ during the heterogeneous photochemical processing of NO₃⁻ in thin liquid films on the Martian surface.

Downward transport of nitrogen (HNO₃(g) and N₂(g))

Figure 4 also shows that there will be downward transport of nitrogen species to the Martian subsurface. In desert environments on Earth, water infiltration and leaching are minimal (Walvoord et al. Reference Walvoord2003; Graham et al. Reference Graham, Hirmas, Wood and Amrhein2008) so the downward transport of atmospheric nitrogen will be dominated by gas-phase diffusion. Because the mean-free paths of HNO₃ and N₂ through the background atmosphere are greater than the typical pore size (∼1 μm), molecular collisions with the walls of the pores dominate the transport of these molecules. This is known as Knudsen diffusion, for which we can take D∼(2εr_o/3τ)(2kT/πm)^1/2, where r_o is the pore size, ε is the porosity, τ is the tortuosity and m is the molecular mass of the diffusing component (Bullock et al. Reference Bullock, Stoker, McKay and Zent1994; Harman & McKay Reference Harman and McKay1995). Consistent with diffusion models of Mars, we use r_o=6×10⁻⁴ cm, ε=0.5 and τ∼5 for depths less than ∼1 km (Squyres et al. Reference Squyres, Clifford, Kuzmin, Zimbelman, Costard, Kieffer, Jakosky, Snyder and Matthews1992; Mellon & Jakosky Reference Mellon and Jakosky1993; Bullock et al. Reference Bullock, Stoker, McKay and Zent1994; Harman & McKay Reference Harman and McKay1995). At a mean surface temperature of 220 K, we find that, above 1 km, ∼0.54 cm² s⁻¹ and ∼0.81 cm² s⁻¹. The maximum sink that could result from the Knudsen diffusion can be estimated by the rate of downward diffusion, F (molecules cm⁻² s⁻¹), specified by F=−D(dn/dz), where n is the number density of the diffusing component (molecules cm⁻³), z is the depth (cm) with the surface set to z=0, D is the diffusion coefficient (cm⁻² s⁻¹) and dn/dz is the density gradient (molecules cm⁻⁴). 1D photochemical simulations show that the number density of HNO₃ and N₂ at Mars' surface is 1.0×10⁵ and 5.81×10¹⁵ molecules cm⁻³, respectively. Thus a putative biotic layer at 10 m depth would produce HNO₃ and N₂ sinks of −54 and −5×10¹² molecules cm⁻² s⁻¹, respectively, which is an ample supply of available nitrogen that can be efficiently transported to the subsurface to support a putative subsurface biosphere.

Fig. 4. Simplified schematic illustrating HNO₃(g) deposition and absorption in thin liquid films on the Martian surface (i.e. regolith (a) and ice (b)), followed by heterogeneous photochemical processing and transport of NO₃⁻, NO₂⁻, NO₂ and NO to lower depths via mobility of thin liquid films to the Martian subsurface.