Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans

Abstract

Chlorarachniophytes are amoeboflagellate algae that acquired photosynthesis secondarily by engulfing a green alga and retaining its plastid (chloroplast). An important consequence of secondary endosymbiosis in chlorarachniophytes is that most of the nuclear genes encoding plastid-targeted proteins have moved from the nucleus of the endosymbiont to the host nucleus. We have sequenced and analyzed 83 cDNAs encoding 78 plastidtargeted proteins from the model chlorarachniophyte Bigelowiella natans (formerly Chlorarachnion sp. CCMP621). Phylogenies inferred from the majority of these genes are consistent with a chlorophyte green algal origin. However, a significant number of genes (Ϸ21%) show signs of having been acquired by lateral gene transfer from numerous other sources: streptophyte algae, red algae (or algae with red algal endosymbionts), as well as bacteria. The chlorarachniophyte plastid proteome may therefore be regarded as a mosaic derived from various organisms in addition to the ancestral chlorophyte plastid. In contrast, the homologous genes from the chlorophyte Chlamydomonas reinhardtii do not show any indications of lateral gene transfer. This difference is likely a reflection of the mixotrophic nature of Bigelowiella (i.e., it is photosynthetic and phagotrophic), whereas Chlamydomonas is strictly autotrophic. These results underscore the importance of lateral gene transfer in contributing foreign proteins to eukaryotic cells and their organelles, and also suggest that its impact can vary from lineage to lineage. molecular evolution ͉ chlorarachniophytes ͉ chloroplast ͉ phylogeny ͉ secondary endosymbiosis

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

“…As expected, a large proportion (207; 59%) of these were green algal in nature, although 45 (22%) were classified as being derived from red algae. This pattern resembles that seen in an early EST-based analysis of B. natans proteins and was attributed to the mixotrophic lifestyle of chlorarachniophyte algae 35 . For G. theta, 508 of 7,451 genes (6.8%) were deemed to be algal in origin (Fig.…”

Origin and Distribution of Calvin Cycle Fructose and Sedoheptulose Bisphosphatases in Plantae and Complex Algae: A Single Secondary Origin of Complex Red Plastids and Subsequent Propagation via Tertiary Endosymbioses

“…1) and a similar red algal origin for this plastidial gene in Bigelowiella seems likely. Comparable cases of HGT have already been reported for these two phagotrophic complex "green algae" (Archibald et al 2003;Petersen et al 2006), and such lineage-specific acquisitions represent the fortuity of gene recruitment (Martin and Herrmann 1998). In this study, we identified two EGTs concerning SBP and plastidtargeted FBP that have important evolutionary implications.…”

“…Cryptophyte and chlorarachniophyte plastids still harbor highly reduced nucleomorphs, which are respectively the remnants of the nucleus of the red and green algal endosymbionts (Douglas et al 2001;McFadden 1997, 2002). With respect to their complex plastids, euglenophytes and chlorarachniophytes constitute the green lineage, whereas haptophytes, heterokonts, cryptophytes, and peridinincontaining dinoflagellates are representatives of the red lineage (Archibald et al 2003;Delwiche 1999;Li et al 2006). The affiliation of the reduced plastids of apicomplexa, including the malaria parasite Plasmodium falciparum, is unclear since both green and red algal ancestries for the apicoplast are controversially discussed (Cai et al 2003;Funes et al 2002Funes et al , 2003Waller et al 2003).…”

How life changes itself: The Read–Write (RW) genome

“…After a symbiogenetic fusion, there is extensive intracellular transfer of DNA from the organelle compartments to the nuclear genome [110,111]. Thus, most of the proteins needed for plastid and mitochondrial function are synthesized from nuclear transcripts in the cytoplasm and have to be reimported into the organelle where they act [112].…”