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Genomic Architecture of the Two Cold-Adapted Genera Exiguobacterium and Psychrobacter: Evidence of Functional Reduction in the Exiguobacterium Antarcticum B7 Genome

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Genomic Architecture of the Two Cold-Adapted Genera Exiguobacterium and Psychrobacter: Evidence of Functional Reduction in the Exiguobacterium Antarcticum B7 Genome GBE Genomic Architecture of the Two Cold-Adapted Genera Exiguobacterium and Psychrobacter: Evidence of Functional Reduction in the Exiguobacterium antarcticum B7 Genome Larissa M. Dias†, Adriana R.C. Folador†,AmandaM.Oliveira,RommelT.J.Ramos,ArturSilva,and Rafael A. Barauna* Laboratory of Genomics and Bioinformatics, Center of Genomics and Systems Biology, Institute of Biological Sciences, Federal University of Para, Belem, PA, Brazil †These authors contributed equally to this work. *Corresponding author: E-mail: [email protected]. Accepted: February 8, 2018 Abstract Exiguobacterium and Psychrobacter are bacterial genera with several cold-adapted species. These extremophiles are com- monly isolated from the same habitats in Earth’s cryosphere and have great ecological and biotechnological relevance. Thus, through comparative genomic analyses, it was possible to understand the functional diversity of these psychrotrophic and psychrophilic species and present new insights into the microbial adaptation to cold. The nucleotide identity between Exiguobacterium genomes was >90%. Three genomic islands were identified in the E. antarcticum B7 genome. These islands contained genes involved in flagella biosynthesis and chemotaxis, as well as enzymes for carotenoid biosynthesis. Clustering of cold shock proteins by Ka/Ks ratio suggests the occurrence of a positive selection over these genes. Neighbor- joining clustering of complete genomes showed that the E. sibiricum was the most closely related to E. antarcticum.Atotal of 92 genes were shared between Exiguobacterium and Psychrobacter. A reduction in the genomic content of E. antarc- ticum B7 was observed. It presented the smallest genome size of its genus and a lower number of genes because of the loss of many gene families compared with the other genomes. In our study, eight genomes of Exiguobacterium and Psychrobacter were compared and analysed. Psychrobacter showed higher genomic plasticity and E. antarcticum B7 presented a large decrease in genomic content without changing its ability to grow in cold environments. Key words: Psychrobacter, Exiguobacterium, cold adaptation, psychrotrophic, comparative genomics, extremophiles. Introduction whereas Exiguobacterium was first described by Collins et al. Several cold-adapted bacterial strains are taxonomically clas- (1983) with the microbiological characterization of the species sified in the genera Exiguobacterium and Psychrobacter E. aurantiacum. (Vishnivetskaya et al. 2000; Rodrigues et al. 2006; Carneiro The genus Exiguobacterium is physiologically more diverse et al. 2012) and are commonly described in environmental than Psychrobacter, and it includes psychrotrophic, meso- studies using microbiological or molecular approaches philic, and moderate thermophilic bacterial species (Rodrigues et al. 2006, 2009; Yadav et al. 2015). Strains of (Vishnivetskaya and Kathariou 2005). Strains of these genera commonly colonize the same ecological niche, Exiguobacterium are commonly isolated from glacial ice, hot expressing genes that produce a cold-adaptive phenotype. springs, the rhizosphere of plants, permafrosts, and tropical Psychrobacter species have been isolated from the deep water and temperate soils (Rodrigues et al. 2006; Rodrigues and of the sea, permafrosts, Antarctic glacial ice, and sediment, Tiedje 2007; Carneiro et al. 2012). Exiguobacterium and among other habitats (Bowman et al. 1997; Shivaji et al. Psychrobacter are phylogenetically distant genera. Whereas 2005; Chaturvedi and Shivaji 2006; Moyer and Morita Exiguobacterium is classified in the phylum Firmicutes, class 2007; Shravage et al. 2007; Rodrigues et al. 2009). The genus Bacilli, and order Bacillales, Psychrobacter isclassifiedinthe Psychrobacter was first described by Juni and Heym (1986), phylum Proteobacteria, class Gammaproteobacteria,order ß The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Genome Biol. Evol. 10(3):731–741. doi:10.1093/gbe/evy029 Advance Access publication February 8, 2018 731 Dias et al. GBE Pseudomonadales, family Moraxellaceae (https://www.name- sibiricum 255-15), CP015731.1 (Exiguobacterium sp. U13- sforlife.com/; last accessed January 20, 2017). Despite their 1), CP006866.1 (Exiguobacterium sp. MH3), CP000082.1 taxonomical classification, both genera have developed mo- (Psychrobacter arcticus 273-4), CP014945.1 (Psychrobacter lecular mechanisms when they are grown in harsh conditions, alimentarius PAMC 27889), CP012678.1 (Psychrobacter ura- such as low temperature environments. tivorans R10.10B), and CP000323.1 (Psychrobacter cryohalo- The mechanisms of adaptation include the following: lentis K5). 1) increased enzymatic catalytic efficiency; 2) production of unsaturated branched-chain fatty acids to maintain mem- General Genomic Comparisons brane fluidity; 3) expression of cold shock proteins that stabi- Initially, all genomes were compared with the genome of E. lize the bacterial cytosol at low temperatures; 4) uptake of antarcticum B7 by BLASTn, generating a ring on the software compatible solutes to maintain the cellular osmotic balance; BRIG v.0.95 (Alikhan et al. 2011). The GenBank file of E. and 5) carotenoid production (Barria et al. 2013; De Maayer antarcticum B7 was manually curated to highlight the main et al. 2014). Because of these metabolic peculiarities, psychro- genes involved in the cold adaptation processes. These genes philic and psychrotrophic bacteria have great biotechnological were indicated in the rings generated by the software, BRIG. appeal and are widely used in studies of biodegradation of Synteny between the genomes was analysed on the software hydrocarbons, antibiotics, and other environmental pollutants Artemis Comparison Tool (ACT) v.13.0.0 (Carver et al. 2005). (Jiang et al. 2014; Bajaj and Slingh 2015). Furthermore, these Genomic Islands (GIs) of E. antarcticum B7 were predicted by micro-organisms are of extreme importance to better under- GIPSy (Soares et al. 2016). Four types of islands were pre- stand the ecological and biogeochemical processes of the dicted: Resistance Island (RI), Pathogenicity Island (PAI), Earth’s cryosphere (Boetius et al. 2015). Symbiotic Island (SI), and Metabolic Island (MI). The thermo- With the advent of Next-Generation Sequencing (NGS) philic specie Exiguobacterium AT1bwasusedasreference. technologies in the last decade, the number of genomes avail- Genes within GIs were compared by BLASTn to the database able in databases has increased. In total, the GenBank data- of Predicted Genome Islands (Pre_GI) using an e-value of 1e- base has 42 genomes of Exiguobacterium, four of which are 05 to determine the main taxonomic hosts of the foreign completely assembled and belong to psychrotrophic or psy- genes. Pre_GI contains a sequence database of genes ac- chrophilic species. Psychrobacter contains 37 deposited quired by horizontal transfer for the Bacteria and Archaea genomes, four of which are completely assembled and be- domains (Pierneef et al. 2015). long to cold-adapted species. Several bioinformatics tools To determine the conservation of cold shock proteins have been developed to compare and analyse this large (CSPs), all sequences were extracted from GenBank files amount of genomic data. Our work presents the results of and a database was created using the script gb2fasta.py of a comparative genomic analysis performed with the genera the BlastGraph v.1.0 program package (Ye et al. 2013). This Exiguobacterium and Psychrobacter. The results obtained database was compared with itself by BLASTp using the pack- helped us understand and visualize the adaptive molecular age Blastall (Altschul et al. 1990). The resulting .xml file con- diversity of these two phylogenetically distant but ecologically taining the similarity scores was analysed in BlastGraph similar cold-adapted genera. software to construct a de Brujin graph where each node represents a protein sequence and the size of the edges rep- Materials and Methods resents the degree of similarity between these sequences (Ye Data Collection et al. 2013). A neighbor-joining tree was calculated in MEGA7 (Kumaretal.2016) using the same data set described above We have carefully reviewed the 79 genomes of both genera for BlastGraph analyses. Sequences were aligned using deposited in GenBank and selected four genomes for each ClustalW before tree calculation. A total of 1,000 replicates genus to perform the comparative analysis. The selection was were calculated. To evaluate the selective pressure on CSP based on two criteria: 1) the “habitat” and “growth temper- genes, the sequences were analysed using the web applica- ature” information contained in the literature or BioSample tion Ka/Ks of the Norwegian Bioinformatics Platform (Siltberg data and 2) the completeness of the genomes. Only psychro- and Liberles 2002). trophic or psychrophilic species with genomes that were completely assembled were selected for analysis. The genome of Exiguobacterium antarcticum B7 was sequenced by our Clustering Analysis research group using a hybrid assembly methodology that To evaluate the functional and nucleotide similarity between used fragments and mate-paired libraries (Carneiro et al. strains of Exiguobacterium
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