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Taxonomic Novelty and Distinctive Genomic Features of Hot Spring Cyanobacteria.

ABSTRACT: Several cyanobacterial species are dominant primary producers in hot spring microbial mats. To date, hot spring cyanobacterial taxonomy, as well as the evolution of their genomic adaptations to high temperatures, are poorly understood, with genomic information currently available for only a few dominant genera, including Fischerella and Synechococcus. To address this knowledge gap, the present study expands the genomic landscape of hot spring cyanobacteria and traces the phylum-wide genomic consequences of evolution in high temperature environments. From 21 globally distributed hot spring metagenomes, with temperatures between 32 and 75°C, 57 medium- and high-quality cyanobacterial metagenome-assembled genomes were recovered, representing taxonomic novelty for 1 order, 3 families, 15 genera and 36 species. Comparative genomics of 93 hot spring genomes (including the 57 metagenome-assembled genomes) and 66 non-thermal genomes, showed that the former have smaller genomes and a higher GC content, as well as shorter proteins that are more hydrophilic and basic, when compared to the non-thermal genomes. Additionally, the core accessory orthogroups from the hot spring genomes of some genera had a greater abundance of functional categories, such as inorganic ion metabolism, translation and post-translational modifications. Moreover, hot spring genomes showed increased abundances of inorganic ion transport and amino acid metabolism, as well as less replication and transcription functions in the protein coding sequences. Furthermore, they showed a higher dependence on the CRISPR-Cas defense system against exogenous nucleic acids, and a reduction in secondary metabolism biosynthetic gene clusters. This suggests differences in the cyanobacterial response to environment-specific microbial communities. This phylum-wide study provides new insights into cyanobacterial genomic adaptations to a specific niche where they are dominant, which could be essential to trace bacterial evolution pathways in a warmer world, such as the current global warming scenario.

SUBMITTER: Alcorta J

PROVIDER: S-EPMC7674949 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Taxonomic Novelty and Distinctive Genomic Features of Hot Spring Cyanobacteria.

Alcorta Jaime J Alarcón-Schumacher Tomás T Salgado Oscar O Díez Beatriz B

Frontiers in genetics 20201105

Several cyanobacterial species are dominant primary producers in hot spring microbial mats. To date, hot spring cyanobacterial taxonomy, as well as the evolution of their genomic adaptations to high temperatures, are poorly understood, with genomic information currently available for only a few dominant genera, including <i>Fischerella</i> and <i>Synechococcus</i>. To address this knowledge gap, the present study expands the genomic landscape of hot spring cyanobacteria and traces the phylum-wid ...[more]

PMID: 33250920

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Project description:Thermosynechococcus is a genus of thermophilic unicellular cyanobacteria that dominates microbial mats in Asian non-acidic hot springs. These cyanobacteria are the major primary producers in their ecological niches and are promising sources of thermostable enzymes for biotechnology applications. To improve our understanding of these organisms, we conducted whole-genome sequencing of a novel strain for comparative analysis with other representatives in the same genus. This newly characterized strain, Thermosynechococcus sp. TA-1, was isolated from the Taian hot springs in Taiwan. Analyses based on average nucleotide identity (ANI) and genome-scale phylogeny suggested that TA-1 and another Taiwanese strain CL-1 belong to a novel species-level taxon. Two metagenome-assembled genomes (MAGs) originated from India represent the sister group, and Thermosynechococcus elongatus PKUAC-SCTE542 from China is the next closest lineage. All cultivated strains and MAGs from Japan form a separate monophyletic clade and could be classified into two species-level taxa. Intriguingly, although TA-1 and CL-1 share 97.0% ANI, the genome alignment identified at least 16 synteny breakpoints that are mostly associated with transposase genes, which illustrates the dynamic nature of their chromosomal evolution. Gene content comparisons identified multiple features distinct at species- or strain-level among these Thermosynechococcus representatives. Examples include genes involved in bicarbonate transportation, nitric oxide protection, urea utilization, kanamycin resistance, restriction-modification system, and chemotaxis. Moreover, we observed the insertion of type II inteins in multiple genes of the two Taiwanese strains and inferred putative horizontal transfer of an asparagine synthase gene (asnB) associated with exopolysaccharides gene cluster. Taken together, while previous work suggested that strains in this genus share a highly conserved genomic core and no clear genetic differentiation could be linked to environmental factors, we found that the overall pattern of gene content divergence is largely congruent with core genome phylogeny. However, it is difficult to distinguish between the roles of phylogenetic relatedness and geographic proximity in shaping the genetic differentiation. In conclusion, knowledge of the genomic differentiation among these strains provides valuable resources for future functional characterization.

Project description:Viruses exert diverse ecosystem impacts by controlling their host community through lytic predator-prey dynamics. However, the mechanisms by which lysogenic viruses influence their host-microbial community are less clear. In hot springs, lysogeny is considered an active lifestyle, yet it has not been systematically studied in all habitats, with phototrophic microbial mats (PMMs) being particularly not studied. We carried out viral metagenomics following in situ mitomycin C induction experiments in PMMs from Porcelana hot spring (Northern Patagonia, Chile). The compositional changes of viral communities at two different sites were analyzed at the genomic and gene levels. Furthermore, the presence of integrated prophage sequences in environmental metagenome-assembled genomes from published Porcelana PMM metagenomes was analyzed. Our results suggest that virus-specific replicative cycles (lytic and lysogenic) were associated with specific host taxa with different metabolic capacities. One of the most abundant lytic viral groups corresponded to cyanophages, which would infect the cyanobacteria Fischerella, the most active and dominant primary producer in thermophilic PMMs. Likewise, lysogenic viruses were related exclusively to chemoheterotrophic bacteria from the phyla Proteobacteria, Firmicutes, and Actinobacteria. These temperate viruses possess accessory genes to sense or control stress-related processes in their hosts, such as sporulation and biofilm formation. Taken together, these observations suggest a nexus between the ecological role of the host (metabolism) and the type of viral lifestyle in thermophilic PMMs. This has direct implications in viral ecology, where the lysogenic-lytic switch is determined by nutrient abundance and microbial density but also by the metabolism type that prevails in the host community. IMPORTANCE Hot springs harbor microbial communities dominated by a limited variety of microorganisms and, as such, have become a model for studying community ecology and understanding how biotic and abiotic interactions shape their structure. Viruses in hot springs are shown to be ubiquitous, numerous, and active components of these communities. However, lytic and lysogenic viral communities of thermophilic phototrophic microbial mats (PMMs) remain largely unexplored. In this work, we use the power of viral metagenomics to reveal changes in the viral community following a mitomycin C induction experiment in PMMs. The importance of our research is that it will improve our understanding of viral lifestyles in PMMs via exploring the differences in the composition of natural and induced viral communities at the genome and gene levels. This novel information will contribute to deciphering which biotic and abiotic factors may control the transitions between lytic and lysogenic cycles in these extreme environments.

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Dataset Information

Taxonomic Novelty and Distinctive Genomic Features of Hot Spring Cyanobacteria.

Publications

Taxonomic Novelty and Distinctive Genomic Features of Hot Spring Cyanobacteria.

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