Molecular complexity of the differential growth of freshwater diatom species along pH gradients

Abstract

This thesis provides a comprehensive overview of the molecular mechanisms responding to a wide range of pH conditions in phylogenetically distinct freshwater diatom species. Diatoms are a remarkably diverse group of eukaryotic algae belonging to the Stramenopiles (Heterokonts). They constitute one of the most dominant and ubiquitous groups in aquatic environments, in which they play significant ecological and biogeochemical roles. Diatoms originated in marine waters around 190 million years ago, and many clades have subsequently invaded freshwater habitats. Given the buffered pH conditions in the ocean, continental pH gradients are likely among the primary drivers of evolutionary change. Freshwater diatoms are highly sensitive to pH changes in their environment. However, there is limited information on the genetic mechanisms underlying their sensitivity to pH and the resulting species segregation along the pH gradient. The main goal of this thesis was to investigate the molecular responses of phylogenetically distant freshwater diatoms to a wide range of pH conditions to elucidate potential adaptive mechanisms determining diatom sensitivity to pH, particularly to acidic environments. To this end, twelve diatom strains were grown under acidic, neutral, and alkaline conditions in a common garden experiment. The twelve strains encompassed a broad phylogenetic range within the raphid pennate clade of diatoms, including species from the genera Nitzschia, Tryblionella, Eunotia, Navicula, Achnanthidium, Gomphonema, and Encyonopsis. The twelve strains exhibited contrasting growth patterns along the pH gradient, with an apparent phylogenetic pH niche conservatism restricted to lower taxonomic ranks and with variable strength among clades. Environmental pH changes among acidic, neutral, and alkaline pH conditions caused the regulation of a myriad of molecular functions and biological processes across diatoms. Many affected proteins were involved in expression tuning in response to stimuli, presumably to meet physiological requirements dictated by environmental factors. This study demonstrates that the responses of known functions to pH changes exhibited substantial strain-specificity despite strains sharing a significant proportion of these functions. This may be a consequence of the substantial genetic differentiation observed across strains. The study also identifies pH-responsive molecules potentially related to proton extrusion, diatom carbon-concentrating mechanisms (CCM), and silica biomineralization. Growth and molecular responses showed that acidic pH is a more ecologically distinct environment than neutral and alkaline pH conditions for diatoms. The distinctiveness of acidic pH as an eco-evolutionary challenge is probably related to the marine ancestry of diatoms and the widespread regional distribution of pH-circumneutral fresh waters across the planet. Survival at acidic pH likely requires the emergence of new adaptations specifically targeted to low pH, which is consistent with mutational randomness playing a relevant role in adaptive evolution. This research is the first essential step for uncovering the mechanisms underlying the diatom sensitivity to pH, which has been overlooked until now despite pH being a main ecological factor of diatom species segregation in inland waters. This study shows remarkable inter-specific variability in responses to pH variation and provides evidence that acidic environments represent a challenging environment for diatoms from an eco-evolutionary perspective. The anthropogenic increase in acidity in freshwater environments further underscores the significance of elucidating the genetic mechanisms underlying pH tolerance, particularly at low pH.

Date of Award	30 Jul 2024
Original language	English
Supervisor	Marisol Felip Benach (Director) & Jordi Catalan Aguila (Director)