Trivalent Phosphorus and Phosphines as Components of Biochemistry in Anoxic Environments

Abstract

Phosphorus is an essential element for all life on Earth, yet trivalent phosphorus (e.g., in phosphines) appears to be almost completely absent from biology. Instead phosphorus is utilized by life almost exclusively as phosphate, apart from a small contingent of other pentavalent phosphorus compounds containing structurally similar chemical groups. In this work, we address four previously stated arguments as to why life does not explore trivalent phosphorus: (1) precedent (lack of confirmed instances of trivalent phosphorus in biochemicals suggests that life does not have the means to exploit this chemistry), (2) thermodynamic limitations (synthesizing trivalent phosphorus compounds is too energetically costly), (3) stability (phosphines are too reactive and readily oxidize in an oxygen (O 2)-rich atmosphere), and (4) toxicity (the trivalent phosphorus compounds are broadly toxic). We argue that the first two of these arguments are invalid, and the third and fourth arguments only apply to the O 2-rich environment of modern Earth. Specifically, both the reactivity and toxicity of phosphines are specific to aerobic life and strictly dependent on O 2-rich environment. We postulate that anaerobic life persisting in anoxic (O 2-free) environments may exploit trivalent phosphorus chemistry much more extensively. We review the production of trivalent phosphorus compounds by anaerobic organisms, including phosphine gas and an alkyl phosphine, phospholane. We suggest that the failure to find more such compounds in modern terrestrial life may be a result of the strong bias of the search for natural products toward aerobic organisms. We postulate that a more thorough identification of metabolites of the anaerobic biosphere could reveal many more trivalent phosphorus compounds. We conclude with a discussion of the implications of our work for the origin and early evolution of life, and suggest that trivalent phosphorus compounds could be valuable markers for both extraterrestrial life and the Shadow Biosphere on Earth.

Phosphine as a Biosignature Gas in Exoplanet Atmospheres

“…There are two proposed explanations for the production of PH3 in anoxic ecosystems (reviewed in Bains et al 2019b;Glindemann et al 1998;Roels et al 2005;Roels and Verstraete 2001;Roels and Verstraete 2004): 1) PH3 is directly produced by anaerobic bacteria from environmental phosphorus. 2) PH3 is indirectly produced by anaerobic bacteria.…”

Computational Infrared Spectroscopy of 958 Phosphorus-Bearing Molecules

“…Pasek et al (2014) proposed that phosphite [H 2 PO 3 ] -2 and hypophosphite [H 2 PO 2 ]are first produced through microbial metabolism, and these compounds are then converted to phosphine by other mechanisms. Bains et al (2019) suggested that, in some environments, it is a combination of phosphate-reducing bacteria and the coupling with phosphite metabolism that results in phosphine release. Several very recent studies are beginning to provide more informed insights into the potential roles of specific microorganisms and pathways in phosphine production.…”

“…The activity of the enzyme dehydrogenase was shown to be positively correlated with phosphine production (Fan et al, 2020b), suggesting that this enzyme's function in producing electrons and reducing agents contributes to phosphine generation. Furthermore, co-factors, such as NADH and riboflavin vitamins were suggested to be key in phosphine production (Bains et al, 2019;Fan et al, 2020b). Given the limited studies and the debate surrounding the exact pathways and the diverse microorganisms potentially involved in phosphine production, significantly more work is needed in this area on the biological basis for phosphine production.…”

Natural Products Containing ‘Rare’ Organophosphorus Functional Groups

“…The detailed biosynthetic pathway for microbial phosphine production is currently unknown. For detailed discussion of the biological production in the environment, its biochemistry, and atmospheric chemistry see three recent papers by Bains, Sousa-Silva and colleagues [ 482 , 494 , 495 ].…”

“…We believe that there could be other biological trivalent phosphorus compounds awaiting discovery. The large majority of ‘natural products’ (i.e., chemicals made by life) are identified from aerobic samples—plants, animals, soil fungi, and Ascomycetes grown in aerated culture—as well as marine organisms [ 494 ]. Very few are collected from anaerobic samples, in part because of the received wisdom among natural product chemists that anaerobic organisms do not produce secondary metabolites [ 497 ].…”