Transcriptional regulation of a horizontally transferred gene from bacterium to chordate

Abstract

The horizontal transfer of genes between distantly related organisms is undoubtedly a major factor in the evolution of novel traits. Because genes are functionless without expression, horizontally transferred genes must acquire appropriate transcriptional regulations in their recipient organisms, although the evolutionary mechanism is not known well. The defining characteristic of tunicates is the presence of a cellulose containing tunic covering the adult and larval body surface. Cellulose synthase was acquired by horizontal gene transfer from Actinobacteria. We found that acquisition of the binding site of AP-2 transcription factor was essential for tunicate cellulose synthase to gain epidermal-specific expression. Actinobacteria have very GC-rich genomes, regions of which are capable of inducing specific expression in the tunicate epidermis as the AP-2 binds to a GCrich region. Therefore, the actinobacterial cellulose synthase could have been potentiated to evolve its new function in the ancestor of tunicates with a higher probability than the evolution depending solely on a spontaneous event.

Structure of native cellulose microfibrils, the starting point for nanocellulose manufacture

“…Cellulose biosynthesis arose in prokaryotes [14,16,17], is best known in plants [14,18], and occurs in an oddly scattered range of other eukaryotes [19][20][21][22], possibly tracing more than one horizontal transfer of cellulose synthase genes and regulatory elements from bacteria [14,23]. Cellulose microfibrils vary greatly in thickness and structure depending on the geometry of the arrays of cellulose synthases that assemble them [21].…”

From morphogenesis to pathogenesis: A cellulose loosening protein is one of the most widely distributed tools in nature

“…Few expansin genes occur in Metazoans (Supplemental Table 3). Tunicates are the only metazoan group known to use cellulose structurally, and acquired their cellulose synthase genes horizontally from bacteria (11, 60, 61). Oiklopeura dioica is the sole tunicate species with a sequenced genome, and it contains an annotated expansin gene.…”

Cellulose production and the evolution of the sessile lifestyle in ascidians

“…To address this question, our group analyzed the enhancer of Ciona intestinalis CesA. The epidermal enhancer of Ci-CesA is simple: it possesses the single binding site of the transcription factor AP-2 (Imai et al, 2017;Ogura and Sasakura 2016) that is necessary for the epidermal expression of Ci-CesA (Sasakura et al, 2016). This simplicity is unusual regarding tissue-specific expression during embryogenesis;…”

“…The binding site of AP-2 is known to be rich in G and C. Particularly, the AP-2 binding site of Ciona CesA is 5′-gcctgcgggc-3′ (Sasakura et al, 2016). Moreover, an approximately 100-base pair DNA stretch that flanks the AP-2 binding site of…”

“…(4) Conservation of the CesA expression mechanism among tunicates. Ciona CesA is expressed in the epidermis in an AP-2-dependent manner (Sasakura et al, 2016). If the CesA expression mechanism was passed on from the ancestor, the mechanism must be retained within…”