Quantitative exploration of the occurrence of lateral gene transfer by using nitrogen fixation genes as a case study

Abstract

Lateral gene transfer (LGT) is now accepted as an important factor in the evolution of prokaryotes. Establishment of the occurrence ofLGT is typically attempted by a variety of methods that includes the comparison of reconstructed phylogenetic trees, the search for unusual GC composition or codon usage within a genome, and identification of similarities between distant species as determined by best BLAST hits. We explore quantitative assessments of these strategies to study the prokaryotic trait of nitrogen fixation, the enzyme-catalyzed reduction of N2 to ammonia. Phylogenies constructed on nitrogen fixation genes are not in agreement with the tree-of-life based on 16S rRNA but do not conclusively distinguish between gene loss and LGT hypotheses. Using a series of analyses on a set of complete genomes, our results distinguish two structurally distinct classes of MoFe nitrogenases whose distribution cuts across lines of vertical inheritance and makes us believe that a conclusive case for LGT has been made.LGT) is the process by which genetic material is transferred between distinct evolutionary lineages. This mechanism contrasts with the Darwinian model of vertical descent, where genetic material is inherited from the preceding generation (1).LGT and integration of the transferred DNA into the recipient organism's chromosome occurs by various extensively studied mechanisms (2).LGT is relatively common among prokaryotes, but less common between prokaryotes and eukaryotes. The spread of the acquired gene(s) in the recipient species population depends on natural selection and͞or neutral genetic drift. For example, a gene that has been laterally transferred may confer antibiotic resistance and therefore provide a selective advantage to the organism in the presence of the antibiotic. It is evident that LGT may occur frequently at the cellular level, but it is more difficult for a transferred gene to be sustained in the population and subsequent generations (3, 4). It is commonly accepted that LGT is a source of genetic diversity and has important evolutionary consequences, but opinions vary on the degree of its influence on microbial evolution (4). This topic is of great current interest among biologists and many methods for detecting probable LGT occurrences have been developed (for reviews, see refs. 1, 3, and 5).The increasing abundance of prokaryotic sequences and completed genomes offers new opportunities to study prokaryotic evolution and LGT. If reconstructed phylogenies from different genes conflict with each other and͞or with well studied evolutionary relationships among the species, then this is commonly taken as a sign of LGT (6, 7). Other methods rely on BLAST searches (8) to detect similar gene sequences between divergent organisms (9, 10) or look for genes with deviations from genome-wide GC or codon composition (11).The criticism of many of the approaches for identifying cases of LGT is that the observations can also be explained by a variety of other reasons, such as inaccurate phylogenetic reconstruc...

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“…Even some of the molecular components of methanogens seem to have been laterally transferred to methane-oxidizing members of the domain Bacteria (33). Nitrogenases appear to have been transferred to oxygenic photosynthetic cyanobacteria late in their evolutionary history, probably from an Archaean source (34), and are widespread among diverse groups of Bacteria and Archaea (35). Ammonia monooxygenase genes that encode the key enzyme required for the oxidation of ammonia to hydroxylamine, a key step of the nitrogen cycle, are also widely distributed (36,37).…”

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