TY - JOUR
T1 - A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH
AU - Cortez, Diego
AU - Neira, Gonzalo
AU - González, Carolina
AU - Vergara, Eva
AU - Holmes, David S.
N1 - Publisher Copyright:
Copyright © 2022 Cortez, Neira, González, Vergara and Holmes.
PY - 2022/3/21
Y1 - 2022/3/21
N2 - The genome streamlining theory suggests that reduction of microbial genome size optimizes energy utilization in stressful environments. Although this hypothesis has been explored in several cases of low-nutrient (oligotrophic) and high-temperature environments, little work has been carried out on microorganisms from low-pH environments, and what has been reported is inconclusive. In this study, we performed a large-scale comparative genomics investigation of more than 260 bacterial high-quality genome sequences of acidophiles, together with genomes of their closest phylogenetic relatives that live at circum-neutral pH. A statistically supported correlation is reported between reduction of genome size and decreasing pH that we demonstrate is due to gene loss and reduced gene sizes. This trend is independent from other genome size constraints such as temperature and G + C content. Genome streamlining in the evolution of acidophilic bacteria is thus supported by our results. The analyses of predicted Clusters of Orthologous Genes (COG) categories and subcellular location predictions indicate that acidophiles have a lower representation of genes encoding extracellular proteins, signal transduction mechanisms, and proteins with unknown function but are enriched in inner membrane proteins, chaperones, basic metabolism, and core cellular functions. Contrary to other reports for genome streamlining, there was no significant change in paralog frequencies across pH. However, a detailed analysis of COG categories revealed a higher proportion of genes in acidophiles in the following categories: “replication and repair,” “amino acid transport,” and “intracellular trafficking”. This study brings increasing clarity regarding the genomic adaptations of acidophiles to life at low pH while putting elements, such as the reduction of average gene size, under the spotlight of streamlining theory.
AB - The genome streamlining theory suggests that reduction of microbial genome size optimizes energy utilization in stressful environments. Although this hypothesis has been explored in several cases of low-nutrient (oligotrophic) and high-temperature environments, little work has been carried out on microorganisms from low-pH environments, and what has been reported is inconclusive. In this study, we performed a large-scale comparative genomics investigation of more than 260 bacterial high-quality genome sequences of acidophiles, together with genomes of their closest phylogenetic relatives that live at circum-neutral pH. A statistically supported correlation is reported between reduction of genome size and decreasing pH that we demonstrate is due to gene loss and reduced gene sizes. This trend is independent from other genome size constraints such as temperature and G + C content. Genome streamlining in the evolution of acidophilic bacteria is thus supported by our results. The analyses of predicted Clusters of Orthologous Genes (COG) categories and subcellular location predictions indicate that acidophiles have a lower representation of genes encoding extracellular proteins, signal transduction mechanisms, and proteins with unknown function but are enriched in inner membrane proteins, chaperones, basic metabolism, and core cellular functions. Contrary to other reports for genome streamlining, there was no significant change in paralog frequencies across pH. However, a detailed analysis of COG categories revealed a higher proportion of genes in acidophiles in the following categories: “replication and repair,” “amino acid transport,” and “intracellular trafficking”. This study brings increasing clarity regarding the genomic adaptations of acidophiles to life at low pH while putting elements, such as the reduction of average gene size, under the spotlight of streamlining theory.
KW - acidophile
KW - chemolithoautotroph
KW - evolution of acid resistance
KW - extremophile
KW - gene gain and loss
KW - genome reduction
KW - genome streamlining
KW - protein size reduction and expansion
UR - http://www.scopus.com/inward/record.url?scp=85127943171&partnerID=8YFLogxK
U2 - 10.3389/fmicb.2022.803241
DO - 10.3389/fmicb.2022.803241
M3 - Article
AN - SCOPUS:85127943171
SN - 1664-302X
VL - 13
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
M1 - 803241
ER -