Nappi, Nunzia (2026) Diversity and adaptations of microbial communities to extreme environments. [Tesi di dottorato]

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Abstract

Geothermal environments represent some of the most extreme natural ecosystems on Earth, characterized by the co-occurrence of high temperatures, wide pH gradients, and elevated concentrations of metals and redox-active chemical species. Within these systems, from the points of hydrothermal fluid emergence to the surrounding areas, strongly heterogeneous ecological microenvironments develop, in which the different domains of life are structured into specialized niches and interact both with one another and with the surrounding geochemistry. The study of geothermal ecosystems therefore provides a unique opportunity to investigate microbial adaptation mechanisms to extreme conditions, the dynamics of microbial trophic networks, and the role of biological communities in major biogeochemical cycles. This PhD thesis lies at the intersection of environmental microbiology, geochemistry, and the physiology of photosynthetic microorganisms, with the aim of investigating how extreme physicochemical gradients influence the structure, function, and interactions of microbial communities in continental geothermal systems. It integrates approaches from microbial ecology, environmental genomics, and experimental physiology, combining the analysis of natural communities with the study of model organisms isolated from extreme environments. Among the wide variety of geothermal settings, particular attention is devoted to thermoacidic environments, which are characterized by the simultaneous presence of extremely low pH values and high temperatures, imposing some of the most selective multistress conditions found in nature. Organisms capable of colonizing these environments constitute a highly specialized subset of microbial biodiversity, whose genetic and metabolic repertoires have been profoundly shaped by evolution to ensure survival under extreme conditions. In the thesis, the conceptual framework of thermoacidic environments is outlined, highlighting the central role of iron and sulfur geochemistry as the primary energy drivers of hydrothermal ecosystems. On this basis, the thesis is structured to progressively address the geological, ecological, and physiological dimensions of life in geothermal systems, moving from a theoretical framework to experimental and ecosystem-scale investigations. The first part of the thesis provides a comprehensive overview of thermoacidic environments and of the organisms that inhabit them, with particular emphasis on the distribution of thermoacidophilic microorganisms across the three domains of life (Chapter 1). This section highlights how archaea, bacteria, and photosynthetic eukaryotes have evolved convergent adaptive strategies to maintain cellular homeostasis under conditions of high acidity, elevated temperatures, and high metal concentrations. A central focus of the thesis is the role of Cyanidiophyceae, currently considered the only photosynthetic eukaryotes capable of thriving stably in environments characterized by extremely low pH and temperatures reaching up to 60 °C. Particular emphasis is placed on the contribution of horizontal gene transfer to the evolution of their metabolic and adaptive capacities. Alongside the theoretical and evolutionary analysis, an experimental investigation is carried out to identify and characterize the prokaryotic communities associated with Cyanidiophyceae, both in laboratory cultures and in natural thermoacidic environments, with the aim of elucidating the ecological and functional interactions that support biofilm stability under extreme conditions (Chapter 2). The analysis of microbial communities is subsequently extended to a broader ecosystem scale through the study of geothermal springs along the Rio Grande Rift (New Mexico, USA) (Chapters 3 and 4). This region represents a natural open-air laboratory where the geological and tectonic history of the rift has promoted the formation of numerous geothermal manifestations distributed along the entire axis of New Mexico, providing a natural gradient of physicochemical conditions. This investigation is conducted using an integrated approach that combines 16S rRNA gene sequencing, shotgun metagenomics, and the cultivation-based isolation of photosynthetic microorganisms, in order to understand how fluid geochemistry controls microbial community structure, functional potential, and interactions between prokaryotes and photosynthetic eukaryotes. In addition to the ecological investigation of natural communities, the thesis includes an experimental component focused on the physiology of extremophilic and non-extremophilic photosynthetic microorganisms under controlled laboratory conditions (Chapter 5). In particular, it examines the role of trace metals, which are essential for the functioning of the photosynthetic apparatus and numerous metabolic processes, and whose availability in geothermal environments can vary drastically across space and time. The investigation of physiological responses to trace metal deprivation provides insight into adaptive mechanisms operating under oligotrophic conditions, establishing a direct link between geochemical constraints and cellular functionality.

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