Group II intron and repeat-rich red algal mitochondrial genomes demonstrate the dynamic recent history of autocatalytic RNAs

Abstract

Background Group II introns are mobile genetic elements that can insert at specific target sequences, however, their origins are often challenging to reconstruct because of rapid sequence decay following invasion and spread into different sites. To advance understanding of group II intron spread, we studied the intron-rich mitochondrial genome (mitogenome) in the unicellular red alga, Porphyridium. Results Analysis of mitogenomes in three closely related species in this genus revealed they were 3–6-fold larger in size (56–132 kbp) than in other red algae, that have genomes of size 21–43 kbp. This discrepancy is explained by two factors, group II intron invasion and expansion of repeated sequences in large intergenic regions. Phylogenetic analysis demonstrates that many mitogenome group II intron families are specific to Porphyridium, whereas others are closely related to sequences in fungi and in the red alga-derived plastids of stramenopiles. Network analysis of intron-encoded proteins (IEPs) shows a clear link between plastid and mitochondrial IEPs in distantly related species, with both groups associated with prokaryotic sequences. Conclusion Our analysis of group II introns in Porphyridium mitogenomes demonstrates the dynamic nature of group II intron evolution, strongly supports the lateral movement of group II introns among diverse eukaryotes, and reveals their ability to proliferate, once integrated in mitochondrial DNA.

Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes

“…Interestingly, the intron contains an intron-encoded protein (IEP) with a reverse transcriptase (RT) domain that is clearly related to IEPs in other red alga-derived plastid genomes, such as those in the group II introns of the dna K, psa A and trn M genes of rhodophytes, ch lB, psa A, and psb B in cryptophytes, in the psa J gene of the green alga-derived plastid genome of euglenoids, as well as various plastid and/or mitochondrial genes in other stramenopiles, fungi, and rhizarians ( Supplementary Figure S5 ). This is consistent with earlier studies documenting the patchy distribution of group II introns in cyanobacteria and diverse eukaryotes (e.g., Odom et al, 2004 ; Sheveleva and Hallick, 2004 ; Khan and Archibald, 2008 ; Kim et al, 2022 ; Suzuki et al, 2022 ). While our phylogenetic analyses failed to identify an obvious donor of the F. japonica psb B intron, it is noteworthy that previous investigation of the mitochondrial genome of the raphidophyte Chattonella marina identified a putative LGT of a group II intron from diatoms to raphidophytes ( Kamikawa et al, 2009 ).…”

“…Detailed speculation on the frequency and directionality of group II intron transfers in eukaryotes is beyond the scope of our study. But we should emphasize that mitochondrial IEPs, such as those analyzed by Kamikawa et al (2009) and Kim et al (2022) , were only rarely retrieved in our BLAST sequence searches ( e- value cutoff = 1e −5 , word size = 6) and are thus poorly represented in the RT / IEP phylogenetic analyses presented herein (the F. japonica plastid psb B intron and the C. marina mitochondrial cox 1 IEP are too distant from one another to allow for meaningful comparison). All these caveats aside, our results are consistent in showing intriguing connections between mobile genetic elements in diatoms and marine raphidophytes.…”

Independent Size Expansions and Intron Proliferation in Red Algal Plastid and Mitochondrial Genomes

“…The mitogenome of the fungus Morchella crassipes (∼500 kb) is the largest known outside plants and is also rich in group II (but also group I) introns ( Liu et al 2020b ). Mitogenome expansion occurs in red algae to a less extreme extent but has resulted in the largest red algal mitochondrial genome (∼132 kb), recently described in a strain of P. purpureum ( Kim et al 2022 ). In this study, we show multiple lineage-specific genome expansions, including a more than 3-fold genome size increase in P. venetus in comparison to C. caeruleus ( fig.…”

Integrating phylogenetics with intron positions illuminates the origin of the complex spliceosome

“…Group II introns are present in several mitochondrial and plastid genomes (Zimmerly et al 2001). Notwithstanding the extent of horizontal gene transfer of these introns among eukaryotes, group II introns were probably present in the mitochondria in LECA (Kim et al 2022). Our analysis did not yield sufficient phylogenetic signal to confidently position PRPF8 in the IEP tree.…”