Migliaccio, Flavia (2026) The entanglement between microbial communities and geochemistry in the light of Italian shallow-water hydrothermal vents. [Tesi di dottorato]

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Abstract

Life on Earth likely emerged within hydrothermal vents during the planet’s early history (Baross and Hoffman, 1985; Martin et al., 2008). In the Archaean eon, approximately four billion years ago, internal heat from planetary accretion and radioactive decay drove intense volcanism and pervasive tectonic deformation that, in combination with the widespread presence of liquid water, promoted vigorous hydrothermal circulation throughout the oceanic crust (Korenaga, 2013; Nisbet and Sleep, 2001). Vents are thus the surface expression of complex subsurface processes involving heat transfer, fluid circulation, and water–rock interactions, affecting metal availability and volatile release (German and von Damm, 2003). Microbial communities exploit metals as catalytic cofactors or structural components of enzymes and proteins (hence designated as biometals), and utilize volcanogenic gases as electron donors and acceptors, thereby harnessing the natural redox disequilibria generated in these systems and ultimately shaping community structure, metabolic potential, and evolutionary trajectories (Amend and Shock, 2001; Hay Mele et al., 2023). Hydrothermal systems offered the geochemical chance for the emergence of life, and life subsequently rendered these conditions a necessity for its own functioning. Hydrothermal vents are widely studied as natural laboratories where subsurface geochemical processes directly structure microbial life (Fullerton et al., 2021; Giovannelli et al., 2021). They sustain ancient and metabolically diverse forms of chemosynthesis, regulate metal and nutrient cycling, inform models of early Earth and planetary habitability, and host underexplored components of modern marine ecosystems with their metabolic potentia (Baross and Hoffman, 1985; Jannasch and Mottl, 1985). Yet our understanding of the hydrothermal vent biosphere and its coupling to the geosphere remains fragmentary and uneven. The landmark 1977 expedition to the Galápagos Rift that discovered deep-sea hydrothermal vents and their astonishing associated biota fundamentally altered prevailing assumptions about the limits of life (Corliss et al., 1979). To what extent do hydrothermal environments still harbour unrecognized biological and metabolic diversity, and how might future exploration further reshape current scientific paradigms? Addressing these questions is essential, as hydrothermal systems provide a unique window into the functioning of our planet and may yield insights relevant to contemporary environmental and societal challenges (Elkassas et al., 2025; Giovannelli et al., 2022; Reveillaud et al., 2016). Within this broader context, the Italian territory represents a particularly compelling natural setting. It is characterized by intense volcanism and tectonic activity resulting from the convergence of the African and Eurasian plates (Antoncecchi and Ceruti, 2015). As a consequence, more than 70 volcanic-associated marine ecosystem sites have been identified in Italian waters, largely concentrated in the Tyrrhenian Sea; however, only a limited number of these systems has been explored in detail (Arcadi et al., 2023; Barosa et al., 2023; Costa et al., 2023). Because hydrothermal circulation is driven by a complex interplay of tectonic, magmatic, and hydrogeological processes, the reactions leading to the formation of hydrothermal fluids vary substantially among sites, rendering each vent end-member fluid highly distinctive in both space and time. Accordingly, the associated microbial diversity—including community composition and the functional potential encoded in microbial genomes—is expected to have adapted to these site-specific and dynamically evolving geochemical conditions over evolutionary timescales. The present PhD thesis aims to advance our understanding of the interactions between the biosphere and the geosphere in geothermal systems, as these environments enable the exploration of both short-term ecological responses and long-term evolutionary adaptations of microbial communities to geochemically dynamic environments. By coupling microbiological and geochemical approaches, this work seeks to disentangle how hydrothermal fluids—through the availability of metals and volcanic gases—shape microbial taxonomic and functional diversity across spatial and temporal scales. I sampled and analysed geothermal emissions including Italian shallow-water hydrothermal vents and worldwide distributed deeply sourced seeps to investigate prokaryotic taxonomic and functional diversity. To elucidate how prokaryotic communities are structured by geochemical conditions, I integrated fluid geochemistry with comparative genomics. All samples analysed in this study are unique and mostly unpublished collections obtained from scientific campaigns between 2017 and 2024. The specific questions addressed in this work include: how do microorganisms regulate biometal homeostasis under extreme and geochemically dynamic conditions? To what extent do subsurface processes and biometal availability affect the diversity and distribution of microbial biometal ions transport systems? Are there correlations between biometal distribution and transporters? Do shallow-water hydrothermal vents exert detectable biogeochemical control beyond the vent orifice, and how far into the surrounding environment can this influence be detected? These questions were addressed at different spatial and temporal scales and with different research focus. The thesis opens with a comprehensive review of microbial biometal transporters, which for the first time organizes their extensive diversity into a unified superfamily-based database. This review addresses key aspects of microbial metal homeostasis, including transporters energetics, metal sensing mechanisms, metallophore-mediated uptake, transporter promiscuity, and shifts in biometal availability over evolutionary time. Biometal homeostasis and the molecular machinery that mediates it are framed as interfaces between intracellular requirements and extracellular metal landscapes, thereby linking microbial physiology to geochemical biometal fluxes (Chapter 1). The subsequent chapter examines the distribution of microbial biometal transporters across geothermal features distributed worldwide, coupling transporter diversity with biometal availability and relevant physico-chemical parameters. A custom and manually curated database of microbial biometal transporter proteins was developed to systematically screen metagenomic datasets. This chapter thus addresses the entanglement between microbiology and geochemistry in volcanic-associated systems at a broad spatial scale, with the observed patterns reflecting long-term evolutionary adaptation of microbial physiology to subsurface processes. Accordingly, the focus is placed on the molecular determinants of biometal homeostasis and their response to environmental constraints, adopting a comparative genomics perspective (Chapter 2). The thesis then shifts to a site-specific investigation of the shallow-water hydrothermal vent system Secca delle Fumose (Gulf of Pozzuoli, Naples), where the interplay between vent geochemistry and microbial community structure is examined at a localized scale. In contrast to the previous chapter, this study captures the immediate ecological effects of hydrothermal fluid emissions on surrounding microbial communities. The taxonomic and functional characterization of vent- and seawater-associated microbiomes, conducted at multiple levels of genomic resolution from read-based profiles to metagenome-assembled genomes (MAGs), emphasizes the role of vent-derived microbial assemblages in local biogeochemical cycling (Chapter 3). Finally, the sampling strategies employed throughout the thesis to link geological processes, metal and volcanic gas delivery, and biological responses across both broad and localized scales are exemplified through a detailed account of the AEO24 expedition conducted across the Aeolian Archipelago (Sicily, Italy) in 2024. This region represents one of the most geothermally active areas in Italy, with Vulcano Island standing among the best characterised hydrothermal vent fields from both the geochemical and the microbiological point of view. Therefore, this latter chapter provides an integrative field framework that connects the approaches and perspectives developed in the preceding ones (Chapter 4).

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