Gene clusters for biosynthesis of mycosporine‐like amino acids in dinoflagellate nuclear genomes: Possible recent horizontal gene transfer between species of Symbiodiniaceae (Dinophyceae)

Abstract

Global warming increases the temperature of the ocean surface, which can disrupt dinoflagellate‐coral symbioses and result in coral bleaching. Photosynthetic dinoflagellates of the family Symbiodiniaceae include bleaching‐tolerant and bleaching‐sensitive coral symbionts. Therefore, understanding the molecular mechanisms for changing symbiont diversity is potentially useful to assist recovery of coral holobionts (corals and their associated microbes, including multiple species of Symbiodiniaceae), although sexual reproduction has not been observed in the Symbiodiniaceae. Recent molecular phylogenetic analyses estimate that the Symbiodiniaceae appeared 160 million years ago and diversified into 15 groups, five genera of which now have available draft genomes (i.e., Symbiodinium, Durusdinium, Breviolum, Fugacium, and Cladocopium). Comparative genomic analyses have suggested that crown groups have fewer gene families than early‐diverging groups, although many genes that were probably acquired via gene duplications and horizontal gene transfers (HGTs) have been found in each decoded genome. Because UV stress is likely a contributor to coral bleaching, and because the highly conserved gene cluster for mycosporine‐like amino acid (MAA) biosynthesis has been found in thermal‐tolerant symbiont genomes, I reviewed genomic features of the Symbiodiniaceae, focusing on possible acquisition of a biosynthetic gene cluster for MAAs, which absorb UV radiation. On the basis of highly conserved noncoding sequences, I hypothesized that HGTs have occurred among members of the Symbiodiniaceae and have contributed to the diversification of Symbiodiniaceae–host relationships. Finally, I proposed that bleaching tolerance may be strengthened by multiple MAAs from both symbiotic dinoflagellates and corals.

Exploring the Relationship between Biosynthetic Gene Clusters and Constitutive Production of Mycosporine-like Amino Acids in Brazilian Cyanobacteria

“…Interestingly, the mys A+ mys B and mys C+ mys D fused copies found in Porphyra umbilicalis served as an outgroup of the clustered version of the mys ABC genes in cyanobacteria, whereas the mys D seems to have a divergent origin, being ancestral to the analogous in red algae [ 49 ]. The history of this gene cluster is still unclear, with gene transfer between bacteria or dinoflagellate or algae possibly playing a major role in its evolution and occurrence [ 41 ]. This could reflect loss of MAA biosynthesis over evolutionary time in these cyanobacteria, with changes in environmental conditions and acclimation.…”

“…Assembly was performed using PhyML [ 38 , 39 ] and tree construction was performed using TreeDyn [ 40 ]. Some non-cyanobacterial sequences ( Dactylococcopsis salina PCC8305, Porphyra umbilicalis , and Chondrus crispus ) known to encode proteins for functional MAA production were included to evaluate the origin and evolutionary history of the cyanobacterial genes [ 41 ].…”

Reversing the directionality of reactions between non-oxidative pentose phosphate pathway and glycolytic pathway boosts mycosporine-like amino acid production in Saccharomyces cerevisiae

“…However, when carbon flux is redirected from glycolytic intermediates to the NOPPP in the pfk2∆ strain, S7P produced through this pathway will be [1- 13 C]-labelled. Transketolase transfers the C1 and C2 carbons of F6P to G3P, producing unlabelled E4P and either [1-13 C]-X5P or [1,[5][6][7][8][9][10][11][12][13] C]-X5P. The C1 and C2 carbons of X5P are then transferred to unlabelled R5P from the oxidative PPP, producing labelled [1-13 C]-S7P (Fig.…”

“…While primary MAAs differ in the type of amino acid substituents attached to the cyclohexenone ring, and absorb UV maximally in the 330-335 nm range, secondary MAAs are produced through modifications to the side chains of primary MAAs. These processes could include esterification, amidation, dehydration, decarboxylation, and nitrogen substitution [8,9]. A few secondary MAAs such as palythene and usujirene absorb maximally at about 360 nm [10].…”

Exploring Mycosporine-like Amino Acid UV-Absorbing Natural Products for a New Generation of Environmentally Friendly Sunscreens

“…Using genome mining approaches [45,[155][156][157], the discovery of MAA biosynthetic pathways occurred through the identification of the gene counterparts in different Gram-positive bacteria [154], cyanobacteria [150,152,156,158,159], and microalgae Symbiodiniaceae [160,161]. All species capable of MAA synthesis were found to have highly similar sequences corresponding to genes from the MAA shikimate or pentose phosphate pathways [160].…”