Paths of lateral gene transfer of lysyl-aminoacyl-tRNA synthetases with a unique evolutionary transition stage of prokaryotes coding for class I and II varieties by the same organisms

Abstract

Background: While the premise that lateral gene transfer (LGT) is a dominant evolutionary force is still in considerable dispute, the case for widespread LGT in the family of aminoacyl-tRNA synthetases (aaRS) is no longer contentious. aaRSs are ancient enzymes, guarding the fidelity of the genetic code. They are clustered in two structurally unrelated classes. Only lysine aminoacyl-tRNA synthetase (LysRS) is found both as a class 1 and a class 2 enzyme (LysRS1-2). Remarkably, in several extant prokaryotes both classes of the enzyme coexist, a unique phenomenon that has yet to receive its due attention.

An Evolutionary Analysis of Lateral Gene Transfer in Thymidylate Synthase Enzymes

“…The evolutionary phenomenon whereby the same archaeon or bacterium encodes 2 structurally distinct enzymes performing the same function is postulated to be a possible transition stage in lateral gene transfer (LGT) and subsequent gene loss ( Doolittle et al 2003 ). We have previously observed and characterized this phenomenon in the context of archaeal and bacterial lysine aminoacyl-tRNA synthetases ( Shaul et al 2006 ).…”

The T box regulatory element controlling expression of the class I lysyl-tRNA synthetase of Bacillus cereus strain 14579 is functional and can be partially induced by reduced charging of asparaginyl-tRNAAsn

“…The T-box element in the B. cereus and B. thuringiensis strains has a canonical structure [ 8 ], is highly conserved and controls expression of a class I LysRS (encoded by the lysK gene) of Pyrococcal origin [ 20 ]. Interestingly, the lysK gene is expressed predominantly during stationary phase in B. cereus strain 14579, whereas the class II LysRS is expressed during exponential growth of this bacterium [ 8 ].…”

“…There are several interesting features about this cohort of T box regulated LysRS: (i) all bacterial species with a T box regulated LysRS have a second LysRS that is not T box regulated; (ii) the four T box elements in the phylogenetically related B. cereus and B. thuringiensis species are associated with a class I LysRS1 and display ~92% identity; (iii) the class I LysRS1 of B. cereus and B. thuringiensis is most closely related to LysRS1 from Pyrococcal species suggesting that a common ancestor of B. cereus/thuringiensis acquired it by a lateral gene transfer event [ 20 ]; (iv) the T box regulated LysRS1 in B. cereus strain 14579 is expressed predominantly in stationary phase [ 8 ] and (v) T box elements do not occur in Archaebacteria . The likely Pyrococcal origin of B. cereus LysRS1 and the absence of T box elements in Archaebacteria presents an interesting question as to how the regulatory sequence and structural gene were conjoined in this case.…”

“…In Bacillus cereus strain 14579, the LysRS2-encoding lysS gene is positioned at the end of an operon encoding genes involved in folate metabolism, its normal position in most Bacilli while the lysK gene encoding the class I-type LysRS1 is located elsewhere on the chromosome. Shaul et al (2006) show that this LysRS1 is closely related to the class I LysRS1 of Pyrococcus , suggesting that it has been acquired by B. cereus by horizontal transfer [ 20 ]. The function of LysRS1 in B. cereus is not clear but it is expressed predominantly in stationary phase and can aminoacylate a novel tRNA species (tRNA Other ) in concert with the class II LysRS enzyme [ 8 ].…”

Genetic Validation of Leishmania donovani Lysyl-tRNA Synthetase Shows that It Is Indispensable for Parasite Growth and Infectivity

“…These enzymes are the validated targets for the development of new antiparasitic agents with novel mechanisms of action ( 6 ). Among all aaRSs, lysyl-tRNA synthetase (LysRS) is unusual because it belongs to either class I or class II enzymes ( 26 ). In most organisms, LysRS is present as the class II form.…”