Comparative genomic analyses of transport proteins encoded within the red algae Chondrus crispus, Galdieria sulphuraria, and Cyanidioschyzon merolae¹¹

Abstract

Galdieria sulphuraria and Cyanidioschyzon merolae are thermo-acidophilic unicellular red algal cousins capable of living in volcanic environments, although the former can additionally thrive in the presence of toxic heavy metals. Bioinformatic analyses of transport systems were carried out on their genomes, as well as that of the mesophilic multicellular red alga Chondrus crispus (Irish moss). We identified transport proteins related to the metabolic capabilities, physiological properties, and environmental adaptations of these organisms. Of note is the vast array of transporters encoded in G. sulphuraria capable of importing a variety of carbon sources, particularly sugars and amino acids, while C. merolae and C. crispus have relatively few such proteins. C. crispus may prefer short chain acids to sugars and amino acids. Additionally, the number of encoded proteins pertaining to heavy metal ion transport is highest in G. sulphuraria and lowest in C. crispus. All three organisms preferentially utilize secondary carriers over primary active transporters, suggesting that their primary source of energy derives from electron flow rather than substrate-level phosphorylation. Surprisingly, the percentage of inorganic ion transporters encoded in C. merolae more closely resembles that of C. crispus than G. sulphuraria but only C. crispus appears to signal via voltage-gated cation channels and possess a Na+, K+-ATPase and a Na+-exporting pyrophosphatase. The results presented in this report further our understanding of the metabolic potential and toxic compound resistances of these three organisms.

Energizing the plasmalemma of marine photosynthetic organisms: the role of primary active transport

“…In the Rhodophyta, the non-marine (acid hot spring) Cyanidium caldarium , Cyanidioschyzon merolae and Galdieria sulphuraria (Cyanidiophyceae) have P-type H + -ATPases but not Na + -ATPases (Ohta et al ., 1997; Lee et al ., 2017). Two Na + -ATPases (PyKPA1 and PyKPA2) have been characterized in the marine bangiophycean Porphyra yezoensis (now Pyropia yezoensis ) (Barrero-Gil et al ., 2005; Uji et al ., 2012 a , 2012 b ; see also Chan et al ., 2012; Kishimoto et al ., 2013).…”

“…It should be noted that the measurement of Ψ CO in the essentially non-vacuolate Porphyra purpurea cells by Reed and co-workers was determined using the distribution of the lipophilic cation TPMP + ; there are reservations about the use of this method of measuring transplasmalemma electrical potential differences in eukaryotes (Ritchie, 1982, 1984). The floridiophycean Chondrus crispus has a P-type Na + -ATPase but no H + -ATPase (Lee et al ., 2017). There seem to be no relevant data for freshwater red algae.…”

Structural and functional comparison of magnesium transporters throughout evolution

“… a The MgtE orthologues have currently only been described in unicellular green and red algae ( Viridiplantae and Archaeplastida , respectively) [ 14 , 15 ] b TRP channels have been described in yeast, but to date no particular orthologues of TRPM6/7 have been identified …”

The Transporter Classification Database (TCDB): 2021 update

“…This has been possible in part because of novel metagenomic data; 36% of the new families in this update include proteins from metagenomes. Moreover, combined with the improvement of software tools and developments in the field, TCDB now provides excellent opportunities to (a) explore relationships between families of transporters ( 5 , 13 , 28–32 , 37 , 40–42 ), (b) characterize and perform comparative analyses of transportomes encoded within genomes and metagenomes ( 14–18 , 22 ) and (c) derive inferences of function to be followed by experimental verification ( 50 ). The characterization of transporter families in TCDB, based on shared domains (tcDoms), allows rapid evaluation of family memberships for individual proteins, identification of evolutionary relationships, and inference of substrates and molecular functions.…”

“…From the 189 families with metagenomic members, 119 (62%) involve transporters of unknown mechanism of action (TC subclass 9.A) and putative transporters (TC subclass 9.B), including 17 families that seem to be exclusive to the newly discovered CPR and Asgard superphyla. Finally, the genomic analyses of some less well characterized eukaryotes such as red algae ( 22 ) as well as the plethora of experimental findings carried out by many research groups, worldwide, has allowed tremendous expansion of TCDB to include both well characterized and uncharacterized (putative) transport systems.…”