4 Metabolic and Taxonomic Diversification in Continental Magmatic Hydrothermal Systems

Maximiliano J. Amenabar, Matthew R. Urschel, and Eric S. Boyd 4 Metabolic and taxonomic diversification in continental magmatic hydrothermal systems 4.1 Introduction Hydrothermal systems integrate geological processes from the deep crust to the Earth’s surface yielding an extensive array of spring types with an extraordinary diversity of geochemical compositions. Such geochemical diversity selects for unique metabolic properties expressed through novel enzymes and functional characteristics that are tailored to the specific conditions of their local environment. This dynamic interaction between geochemical variation and biology has played out over evolutionary time to engender tightly coupled and efficient biogeochemical cycles. The timescales by which these evolutionary events took place, however, are typically inaccessible for direct observation. This inaccessibility impedes experimentation aimed at understanding the causative principles of linked biological and geological change unless alternative approaches are used. A successful approach that is commonly used in geological studies involves comparative analysis of spatial variations to test ideas about temporal changes that occur over inaccessible (i.e. geological) timescales. The same approach can be used to examine the links between biology and environment with the aim of reconstructing the sequence of evolutionary events that resulted in the diversity of organisms that inhabit modern day hydrothermal environments and the mechanisms by which this sequence of events occurred. By combining molecular biological and geochemical analyses with robust phylogenetic frameworks using approaches commonly referred to as phylogenetic ecology [1, 2], it is now possible to take advantage of variation within the present – the distribution of biodiversity and metabolic strategies across geochemical gradients – to recognize the extent of diversity and the reasons that it exists. The distribution of organisms and their metabolic functions in modern environments is rooted in the selection for physiological adaptations that allowed variant populations to radiate into new ecological niches. Such radiation events are recorded in extant organismal distribution patterns (e.g. habitat range), as well as in the genetic record of the organisms as they are distributed along environmental gradients [3, 4]. These patterns are the result of vertical descent, which is a primary means by which organisms inherit their metabolic or physiological potential from their ancestors, although horizontal gene transfer (HGT), gene loss, and gene fusions are also likely to influence extant distribution patterns. Overall, these phenomena manifest as a posi- Maximiliano J. Amenabar, Matthew R. Urschel: These authors contributed equally to this work 58 | 4 Biodiversity of continental hydrothermal systems Fig. 4.1. Universal tree of life, overlain with maximum growth temperature, implies a thermophilic origin of life (adapted from Lineweaver and Schwartzman, 2004 [14]). tive relationship between the physiological, ecological, and evolutionary relatedness of organisms [1, 2, 5, 6]. The correlation between the phylogenetic relatedness of microbial taxa and their overall ecological similarity allows an analysis of the overall phylogenetic relatedness and structure of communities of interacting organisms to be used to investigate the contemporary ecological processes that structure their composition [1]. The aforementioned attributes of biological systems offer ‘a window into the past’ as extant patterns in the distribution of species or metabolic function can be used to infer historical constraints imposed by the environment on the diversification of species and/or metabolic function [7–13]. Most phylogenetic studies conducted on early life have used gene or protein sequence data obtained from culture collections making it difficult to place results inan ecological context. For example, phylogenetic reconstructions of contemporary genes or proteins indicate that the first forms of life ( Fig. 4.1) [14] and many of the physiological functions that sustained it (e.g. hydrogen oxidation [15]) may have a hydrothermal heritage. Additional evidence in support of a thermophilic character for early forms of life for this suggestion comes from an analysis of resurrected proteins that are likely to share attributes of the last universal common ancestor (LUCA) of Archaea and Bacte- ria. Biochemical characterization of these proteins indicates that they function more efficiently at elevated temperatures than they do at mesophilic temperature [16]. This is consistent with the elevated temperatures predicted by silicon and oxygen isotope data for near surface environments in Archean oceans based on silicon and oxygen isotopic data (55 °C to 85 °C) [17–19]. However, more recent studies based on phos- phate isotopic data suggest that Archean oceans were clement (< 40 °C) [20]. While this seems contradictory to the aforementioned phylogenetic and molecular recon- struction data, it is consistent with other phylogenetic studies of ribosomal RNAs that suggest LUCA was a mesophilic organism which then evolved to form the thermophilic ancestor of Bacteria and Archaea [21, 22]. Clearly, there is much still to be learned about the nature of early forms of life on Earth and the characteristics of the environment that drove its emergence and early evolution. 4.2 Geochemistry of hydrothermal systems | 59 The variation in the geochemical composition of present day hydrothermal environments likely encompasses much of the geochemical compositional space that was present on early Earth [23], when key metabolic processes (e.g. methanogenesis, iron reduction, sulfur metabolism, and photosynthesis) that sustain populations inhabiting these systems are thought to have evolved. Geochemical variation in modern hydrothermal environments provides an ideal field laboratory for examination of the natural distribution of taxa, their metabolic functionalities, and for defining the range of geochemical conditions tolerated at the taxonomic and metabolic levels (i.e. habitat range or zone of habitability) [24, 25]. Approaches that integrate molecular biological and geochemical data collected simultaneously within an evolutionary framework can potentially provide new insights into the factors that drove the diversification of metabolic processes that sustain life in hydrothermal environments. The studies reviewed here are aimed at providing a better understanding of the interplay between the geological processes that fuel hydrothermal systems, the characteristics of the modern-day inhabitants of these systems, and the role that geological processes have played in shaping the diversification of ancestral populations that inhabited hydrothermal systems on ancient Earth. In doing so, this chapter will bring together topics on geology, geochemistry, microbial physiology, and phylogenetics to explore the taxonomic and metabolic evolution of microorganisms in continental magmatic systems in the context of the geochemically variable hydrothermal environments that they occupy. 4.2 Geological drivers of geochemical variation in continental hydrothermal systems Hydrothermal systems form as the result of the interaction between magmatic fluid and a heat source. Three key components are required for the formation of a hydrothermal system: a source of water, a source of heat, and permeability of the rock strata overlying the heat source [26]. Although water sources, heat sources, and bedrock permeability may vary across hydrothermal systems, they all include the following gen- eral features: 1) a recharge area where water enters the system from the surface; 2) a subsurface network allowing this water to descend, come into contact with the heat source, and leach minerals from surrounding rock to form hydrothermal fluids; and 3) a discharge area where newly-formed hydrothermal fluids driven to the surface by heat-induced pressure or density changes emerge on the surface to form hydrothermal features such as hot springs, geysers, fumaroles, or mudpots. Magmatic gases such as hydrogen, carbon dioxide, methane, and hydrogen sulfide play an important role in the chemistry of hydrothermal fluids in both marine and continental systems. Since many of these gases drive chemotrophic microbial metabolisms [25, 27, 28], it is essen- tial to understand the distribution and metabolic diversity of microbial life inhabiting these systems. Moreover, abiotic synthesis reactions, as recently reviewed by McCol- 60 | 4 Biodiversity of continental hydrothermal systems Fig. 4.2. Schematic illustrating the hypothesized functioning of a continental magmatic hydrothermal system. Meteoric water infiltrates the subsurface where it is heated by a magma chamber. Less dense heated water returns to the surface. During flow back to the surface, heated water leaches various minerals from different bedrock types. Ascending water can also undergo phase transitions leading to acidic fumaroles and acid-sulfate springs or alkaline high chloride springs. lum and Seewald [29], are capable of producing a variety of reduced hydrocarbons (e.g. formate, carbon monoxide, methane) that likely support chemotrophic populations in hydrothermal ecosystems. Hydrothermal systems are typically classified according to the heat source which drives them. Those systems driven by heat from volcanic activity are termed “magmatic” (e.g. Yellowstone National Park (YNP), USA; Kamchatka, Russia;

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