Evolutionary links between intra‐ and extracellular acid–base regulation in fish and other aquatic animals

Abstract

The acid-base relevant molecules carbon dioxide (CO2), protons (H + ), and bicarbonate (HCO3 -) are substrates and end products of some of the most essential physiological functions including aerobic and anaerobic respiration, ATP hydrolysis, photosynthesis, and calcification. The structure and function of many enzymes and other macromolecules are highly sensitive to changes in pH, and thus maintaining acidbase homeostasis in the face of metabolic and environmental disturbances is essential for proper cellular function. On the other hand, CO2, H + and HCO3have regulatory effects on various proteins and processes, both directly through allosteric modulation and indirectly through signal transduction pathways. Life in aquatic environments 2 presents organisms with distinct acid-base challenges that are not found in terrestrial environments. These include a relatively high CO2 relative to O2 solubility that prevents internal CO2/HCO3accumulation to buffer pH, a lower O2 content that may favor anaerobic metabolism, and variable environmental CO2, pH and O2 levels that require dynamic adjustments in acid-base homeostatic mechanisms. Additionally, some aquatic animals purposely create acidic or alkaline microenvironments that drive specialized physiological functions. For example, acidifying mechanisms can enhance O2 delivery by red blood cells, lead to ammonia trapping for excretion or buoyancy purposes, or lead to CO2 accumulation to promote photosynthesis by endosymbiotic algae. On the other hand, alkalinizing mechanisms can serve to promote calcium carbonate skeletal formation. This non-exhaustive review summarizes some of the distinct acid-base homeostatic mechanisms that have evolved in aquatic organisms to meet the particular challenges of this environment.

Survival, Growth, and Development in the Early Stages of the Tropical Gar Atractosteus tropicus: Developmental Critical Windows and the Influence of Temperature, Salinity, and Oxygen Availability

“…However, there is little information regarding salinity and their early life stages and available information exists only for juveniles and adults [59][60][61][62][63][64]. Lack of maturity of their ionoregulatory and osmoregulatory organs likely explains why newly hatched larvae in the present study could not cope with environmental salinities that could be easily tolerated by adults, since gills are the principal organ for iono/osmoregulation in larval fishes [65][66][67][68]. Atractosteus tropicus has visible gills at hatch, but regular gill ventilation did not start until~5 dph [37].…”

Marine heatwaves depress metabolic activity and impair cellular acid-base homeostasis in reef-building corals regardless of bleaching susceptibility

“…This interaction may therefore increase the potential for ocean acidification to compound the harm of temperature stress on corals and exacerbate bleaching (Dove et al 2020; Gibbin et al 2015), especially because these animals are already living at the upper edge of their thermal tolerance windows. Furthermore, if pH i in corals is regulated more tightly than extracellular body fluids (pH e ) during stress, as it is in other marine invertebrates (Tresguerres et al 2020), the interactive effects of temperature stress and hypercapnia on pH i and pH e regulation may be particularly detrimental for biomineralization, which occurs in extracellular pockets of fluid located between the coral epidermis and the skeleton. Indeed, recent work has found that heat stress impairs coral regulation of calcifying fluid pH e with concurrent declines in calcification (Guillermic et al 2021; Schoepf et al 2021), which raises the question of whether maintenance of coral pH i may be occurring at the expense of pH e during stress.…”

“…Declines in metabolic performance due to heat stress can also trigger changes in cellular processes such as acid-base regulation of intracellular and external body fluids (H. Pörtner 2008). Maintaining a steady pH is crucial for all living organisms, as nearly all metabolic processes require a narrow pH range in order to function (Tresguerres et al 2020). Thus, characterizing the influence of temperature on acid-base homeostasis mechanisms is essential for understanding coral physiological responses to a changing climate.…”

Intracellular pH regulation: characterization and functional investigation of H+ transporters in Stylophora pistillata

“…Vacuolar-type electrogenic H + -ATP hydrolases (V-ATPases), which transport H + via V 0 V-ATPase subunit-a [ 26 ], and plasma membrane Ca + 2 -ATPase (PMCA), which extrudes Ca + 2 in exchange for H + [ 19 , 27 , 28 ], belong to this group. Although some studies claim that pH i regulation is not the primary role of these H + pumps in most mammalian cells [ 19 ], others have suggested the opposite [ 29 – 32 ]. Members of the last group, the H + channels, allow H + to passively diffuse down its electrochemical gradient whenever the regulatory gate is open and includes voltage-gated proton channels (H v CN) [ 33 , 34 ].…”