The environmental adaptation of acidophilic archaea: promotion of horizontal gene transfer by genomic islands

Abstract

Acid mine drainage (AMD) is an extremely acidic leachate highly contaminated with metal ions, yet it harbors a significantly high abundance of archaea. Genomic islands (GIs), as one of the productions of horizontal gene transfer (HGT), play an important role in the environmental adaptation and evolutionary processes of archaea. However, the distribution, structure, and function of GI within the genomes of archaea remain poorly understood. In this study, through the bioinformatic analysis of archaea in AMD, including Ferroplasma acidiphilum ZJ isolated from laboratory and 25 acidophilic archaea collected from NCBI database, 176 GIs were predicted and annotated. Furthermore, we analyzed their structural features and provided insights into the role of HGT in environmental adaptation. The size and distribution of GIs in the genomes were found to be random. In the majority of GIs, the GC content was lower than the average GC content of the strain genome, suggesting that GIs were typically looped out of the genomes with poor stability and transferred into those with higher stability. tRNAs with classical stem-loop secondary structures have been found at the ends of several GIs, suggesting that GIs frequently integrate near tRNAs. In contrast to functional genes directly involved in cellular life processes, GIs were more likely to carry genes related to genetic information and metabolism. Several GIs were identified to carry genes involved in iron oxidation, mercury reduction, and various toxin-antitoxin systems, which enhance the adaptability of the strains to highly acidic environments.

Keywords: Acid mine drainage; Archaea; Environmental adaptation; Genomic island; Horizontal gene transfer.

Fig. 1

a Distribution map of GIs in genome. b The number of GIs in each strain and the number of genes contained in GIs of each strain

Fig. 2

Patterns of GIs in AMD archaea genomes. a Linear regression analysis between number of GIs per archaea genome with GI size (in kb). b Relationship between genome size and number of GIs. c Relationship between archaea genome and GI size. And d Box and whiskers graphic of the GI ratio for the AMD archaea

Fig. 3

a-f Secondary structure of flanked tRNAs. g Marginal histogram of GI size with flanked tRNA and its GC content

Fig. 4

Multiple sequence alignment among the flanked tRNA sequences

Fig. 5

Comparison of average GC content of Genome and GC content of each GI

Fig. 6

COG classification of genes in GIs. Category J, K and L belong to information storage and processing; category D, M, N, O, T, U, Z, and C belong to cellular processes and signaling; category E, F, G, H, I, P and Q belong to metabolism

Fig. 7

Genetic physical map of GIs related to enhance stress resistance