Comparative Plastid Genomics of Cryptomonas Species Reveals Fine-Scale Genomic Responses to Loss of Photosynthesis

Abstract

Loss of photosynthesis is a recurring theme in eukaryotic evolution. In organisms that have lost the ability to photosynthesize, nonphotosynthetic plastids are retained because they play essential roles in processes other than photosynthesis. The unicellular algal genus Cryptomonas contains both photosynthetic and nonphotosynthetic members, the latter having lost the ability to photosynthesize on at least three separate occasions. To elucidate the evolutionary processes underlying the loss of photosynthesis, we sequenced the plastid genomes of two nonphotosynthetic strains, Cryptomonas sp. CCAC1634B and SAG977-2f, as well as the genome of the phototroph Cryptomonas curvata CCAP979/52. These three genome sequences were compared with the previously sequenced plastid genome of the nonphotosynthetic species Cryptomonas paramecium CCAP977/2a as well as photosynthetic members of the Cryptomonadales, including C. curvata FBCC300012D. Intraspecies comparison between the two C. curvata strains showed that although their genome structures are stable, the substitution rates of their genes are relatively high. Although most photosynthesis-related genes, such as the psa and psb gene families, were found to have disappeared from the nonphotosynthetic strains, at least ten pseudogenes are retained in SAG977-2f. Although gene order is roughly shared among the plastid genomes of photosynthetic Cryptomonadales, genome rearrangements are seen more frequently in the smaller genomes of the nonphotosynthetic strains. Intriguingly, the light-independent protochlorophyllide reductase comprising chlB, L, and N is retained in nonphotosynthetic SAG977-2f and CCAC1634B. On the other hand, whereas CCAP977/2a retains ribulose-1,5-bisphosphate carboxylase/oxygenase-related genes, including rbcL, rbcS, and cbbX, the plastid genomes of the other two nonphotosynthetic strains have lost the ribulose-1,5-bisphosphate carboxylase/oxygenase protein-coding genes.

Comparative Plastid Genomics of Non-Photosynthetic Chrysophytes: Genome Reduction and Compaction

“…The rbc - gene present only in certain species is colored light brown. The data were derived from previously published studies ( Donaher et al., 2009 ; Kamikawa et al., 2015 ; Kim et al., 2017 ; Dorrell et al., 2019 ; Kim et al., 2019 ; Tanifuji et al., 2020 ; this study).…”

“…The rbc-gene present only in certain species is colored light brown. The data were derived from previously published studies (Donaher et al, 2009;Kamikawa et al, 2015;Kim et al, 2017;Dorrell et al, 2019;Kim et al, 2019;Tanifuji et al, 2020; this study). photosynthetic organisms such as the colorless euglenoid Euglena longa, the pet genes are all missing (Gockel and Hachtel, 2000).…”

“…The colorless diatom Nitzschia sp. retains a few reduced thylakoid membranes in the plastid stroma and ATP synthase complex and TAT genes (Kamikawa et al, 2015), whereas the colorless cryptophyte Cryptomonas paramecium does not appear to possess any thylakoid membranes (Sepsenwol, 1973) but has retained many of its ATP synthase complex genes (Donaher et al, 2009;Tanifuji et al, 2020).…”

“…Colorless cryptophytes and diatoms (Nitzschia spp.) possess the gene (Dorrell et al, 2019;Tanifuji et al, 2020), but "Spumella" sp. NIES-1846 has lost it.…”

“…( Knauf and Hachtel, 2002 ; Borza et al., 2005 ; Suzuki et al., 2018 ), the parasitic plant Epifagus virginiana ( de Pamphilis and Palmer, 1990 ), members of the free-living green algal genus Polytoma ( Nedelcu, 2001 ; Figueroa-Martinez et al., 2017 ), and the euglenoid alga Euglena longa ( Gockel and Hachtel, 2000 ). Additionally, genome-containing non-photosynthetic plastids of red-algal secondary endosymbiotic origin are diverse in nature, and can be found in the malaria parasite Plasmodium falciparum ( Wilson et al., 1996 ; Waller and McFadden, 2005 ), the cryptophyte Cryptomonas paramecium ( Donaher et al., 2009 ; Tanifuji et al., 2020 ), the colorless diatom Nitzschia species. ( Kamikawa et al., 2018 ), and the chrysophyte “ Spumella ” sp.…”