Geosphere and Biosphere coevolution: the role of trace metals availability in the evolution of biogeochemistry

Abstract

Earth’s geosphere and biosphere have coevolved over time, influencing each other’s stability and keeping our planet habitable for most of its 4.543 billion years of history. Biogeochemical cycles play a key role in controlling this interaction, connecting long-term geological cycles and the much faster evolution of the Earth’s outer biologically dominated envelopes. A small set of microbial-encoded proteins containing redox-sensitive transition metals as their core catalytic center carry out the majority of the key biogeochemical reactions. Metals such as Fe, Co, Ni, Zn, Mo, W, V, and Cu are used in these proteins to access diverse redox couples as a function of the changing planetary availability of these elements over time. Despite the importance of this process, the relationship between metal availability and metabolism evolution and diversity has not been investigated in detail. I pose that elucidating the impact of transition metal availability on microbial functional diversity holds the key to understanding the co-evolution of life and our planet, potentially unlocking a number of important discoveries at the core of diverse fields such as earth sciences, astrobiology, microbial ecology, and biotechnology.

Standard Operating Procedure for the analysis of trace elements in hydrothermal fluids by Inductively Coupled Plasma Mass Spectrometry (ICP-MS)

“…This Standard Operating Procedure (SOP) was developed in the Giovannelli Lab at the Department of Biology of the University of Naples Federico II and outlines the analysis of trace elements involved in biogeochemical cycles from solid and liquid matrices using inductively coupled plasma mass spectrometry (ICP-MS). Although trace metals are recognized as important for microbial metabolism, they are not classically considered as the main factors that drive functional microbial diversity (Giovannelli 2022). Generally, microbial diversity is linked to environmental main physical-chemical parameters, such as temperature, pH, pressure, salinity, O 2 availability or substrates (Delgado-Baquerizo et al 2018).…”

“…The role of metals in influencing biodiversity has been studied classically in the context of their toxicity. In contrast, information on minimum concentration requirements for specific trace elements is severely limited and very few studies have investigated their role in microbial functional diversity control (Morel and Price 2003;Bertrand et al 2007;Giovannelli 2022). Microorganisms play a crucial role in biogeochemical cycles as they are involved in redox reaction, processes that clearly alter the composition of biosphere and geosphere, which have evolved over time, influencing each other.…”

“…Traditional trace elements analysis of geothermal waters focuses on elements that are used to understand geochemical processes mainly linked to the source of the fluids (Féraud et al 2009), the extent of water-rock interactions (Grandell et al 2016) or the presence of anomalies of economically valuable metals also in the future market of clean energy technology such as gold, lithium, cobalt (Gianelli and Grassi 2001). Comparatively less attention has been devoted to the biologically relevant elements (Giovannelli 2022), and very often datasets lack information on rock composition, fluid geochemistry involving the key biological elements such as molybdenum, vanadium or cobalt. Here we describe the standard operating procedures (SOP) developed to routinely analyze such a wide range of fluid and sediments obtained from deeply-sourced springs.…”

“…In our laboratory we routinely quantify biometal such as V, Mn, Fe, Co, Ni, Cu, As, Se, Mo, Cd and W (Giovannelli 2022), and other elements such as Ti, Cr, Ga, Rb, Sr, Zr, Nb, Ag, Cs, Ba, Ta, Re, Tl, Pb, U. Moreover, in the next future we will also quantify rare earth elements such as Ce, Dy, Er, Eu, Gd, Ho, La, Lu, Nd, Pr, Sm, Th, Tm, Y, Yb.…”

Oxidoreductases and metal cofactors in the functioning of the earth

“…Under these criteria, the number of biogeochemically-relevant metal-containing oxidoreductases involved in key steps of the CHNOS cycles is reduced to 59 ( Table 1 and Supplementary Figure S1). These effectively control the biogeochemistry at the interface between the geosphere and biosphere and are more likely to be influenced by the environmental availability of their metal cofactor [ 11 ].…”