Juan J. Roda-García

Universitat de Miguel Hernández d'Elx

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Francisco Rodríguez‐Valera

Universitat de Miguel Hernández d'Elx

Antonio Picazo

Universitat de València

Pedro J. Cabello‐Yeves

Universitat de Miguel Hernández d'Elx

Cristiana Callieri

National Research Council

Antonio Camacho

Universitat de València

Lena Schallenberg

University of Otago

Richard J. Puxty

University of Warwick

Paula Martin De Prado

University of Warwick

David J. Scanlan

University of Warwick

Paula Huber

Universidade Federal de São Carlos

Cooperative Institutions

Universitat de Miguel Hernández d'Elx

University of Warwick

Water Research Institute

National Research Council

University of Alicante

ETH Zurich

Institut de Biologia Evolutiva

Universitat de València

Institute of Oceanology

Bulgarian Academy of Sciences

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Additional file 9 of Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates

Figshare (2022)

Pedro J. Cabello‐Yeves Cristiana Callieri Antonio Picazo Lena Schallenberg Paula Huber

Additional file 9: Table S3. S metabolism. Gene/protein presence/absence between all 132 compared culture derived marine, brackish and freshwater picocyanobacteria. Annotation assessed by Cyanorak CK clusters. CDD was used to retrieve the PSSM-ids from best specific/non-specific hits covering >50 % of the protein.

10.6084/m9.figshare.20454718

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Ecogenomics of the SAR11 clade

Environmental Microbiology (2019)

José M. Haro-Moreno Francisco Rodríguez‐Valera Riccardo Rosselli Francisco Martínez-Hernández Juan J. Roda-García

Summary Members of the SAR11 clade, despite their high abundance, are often poorly represented by metagenome‐assembled genomes. This fact has hampered our knowledge about their ecology and genetic diversity. Here we examined 175 SAR11 genomes, including 47 new single‐amplified genomes. The presence of the first genomes associated with subclade IV suggests that, in the same way as subclade V, they might be outside the proposed Pelagibacterales order. An expanded phylogenomic classification together with patterns of metagenomic recruitment at a global scale have allowed us to define new ecogenomic units of classification (genomospecies), appearing at different, and sometimes restricted, metagenomic data sets. We detected greater microdiversity across the water column at a single location than in samples collected from similar depth across the global ocean, suggesting little influence of biogeography. In addition, pangenome analysis revealed that the flexible genome was essential to shape genomospecies distribution. In one genomospecies preferentially found within the Mediterranean, a set of genes involved in phosphonate utilization was detected. While another, with a more cosmopolitan distribution, was unique in having an aerobic purine degradation pathway. Together, these results provide a glimpse of the enormous genomic diversity within this clade at a finer resolution than the currently defined clades.

Subclade

10.1111/1462-2920.14896

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Citations (89)

Phylogenomics of SAR116 clade reveals two subclades with different evolutionary trajectories and important role in the ocean sulfur cycle

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Juan J. Roda-García José M. Haro-Moreno Lukas A. Huschet Francisco Rodríguez‐Valera Mario López‐Pérez

ABSTRACT The SAR116 clade within the class Alphaproteobacteria represents one of the most abundant groups of heterotrophic bacteria inhabiting the surface of the ocean. The small number of cultured representatives of SAR116 (only two to date) is a major bottleneck that has prevented an in-depth study at the genomic level to understand the relationship between genome diversity and its role in the marine environment. In this study, we use all publicly available genomes to provide a genomic overview of the phylogeny, metabolism and biogeography within the SAR116 clade. This increased genomic diversity revealed has led to the discovery of two subclades of SAR116 that, despite having similar genome size ( ca . 2.4 Mb) and coexist in the same environment, display different properties in their genomic make up. One represents a novel subclade for which no pure cultures have been isolated and is composed mainly of single-amplified genomes (SAGs). Genomes within this subclade showed convergent evolutionary trajectories with more streamlining features, such as low GC content ( ca . 30%), short intergenic spacers (<22 bp) and strong purifying selection (low d N /d S ). Besides, they were more abundant in metagenomic databases recruiting also at the deep chlorophyll maximum. Less abundant and restricted to the upper photic layers of the global ocean, the other subclade of SAR116, enriched in MAGs, accommodated the only two pure cultures. Genomic analysis suggested that both clades have a significant role in the sulfur cycle with differences in the way in which both clades can metabolize the dimethylsulfoniopropionate (DMSP). IMPORTANCE SAR116 clade of Alphaproteobacteria is an ubiquitous group of heterotrophic bacteria inhabiting the surface of the ocean, but the information about their ecology and population genomic diversity is scarce due to the difficulty of getting pure culture isolates. The combination of single-cell genomics and metagenomics has become an alternative approach to study this kind of microbes. Our results expand the understanding of the genomic diversity, distribution, and lifestyles within this clade and provide evidence of different evolutionary trajectories in the genome make-up of the two subclades that could serve to understand how evolutionary pressure can drive different adaptations to the same environment. Therefore, the SAR116 clade represents an ideal model organism for the study of the evolutionary streamlining of genomes in microbes that have relatively close relatedness to each other.

Subclade

Phylogenomics

Alphaproteobacteria

10.1101/2021.05.06.443042

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Additional file 14 of Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates

Figshare (2022)

Pedro J. Cabello‐Yeves Cristiana Callieri Antonio Picazo Lena Schallenberg Paula Huber

Additional file 14: Table S7. Amino acid metabolism. Gene/protein presence/absence between all 132 compared culture derived marine, brackish and freshwater picocyanobacteria. Annotation assessed by Cyanorak CK clusters. CDD was used to retrieve the PSSM-ids from best specific/non-specific hits covering >50 % of the protein.

10.6084/m9.figshare.20454667

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Additional file 19 of Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates

Figshare (2022)

Pedro J. Cabello‐Yeves Cristiana Callieri Antonio Picazo Lena Schallenberg Paula Huber

Additional file 19: Table S11. Reactive oxygen species (ROS). Gene/protein presence/absence between all 132 compared culture derived marine, brackish and freshwater picocyanobacteria. Annotation assessed by Cyanorak CK clusters. CDD was used to retrieve the PSSM-ids from best specific/non-specific hits covering >50 % of the protein.

10.6084/m9.figshare.20454682

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Additional file 2 of The microbiome of the Black Sea water column analyzed by shotgun and genome centric metagenomics

Figshare (2021)

Pedro J. Cabello‐Yeves Cristiana Callieri Antonio Picazo Maliheh Mehrshad José M. Haro-Moreno

Additional file 2: Table S2. Main features and statistics of Black Sea retrieved MAGs.

Shotgun

10.6084/m9.figshare.14228198

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Additional file 21 of Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates

Figshare (2022)

Pedro J. Cabello‐Yeves Cristiana Callieri Antonio Picazo Lena Schallenberg Paula Huber

Additional file 21: Table S12. Mobile genetic elements. Gene/protein presence/absence between all 132 compared culture derived marine, brackish and freshwater picocyanobacteria. Annotation assessed by Cyanorak CK clusters. CDD was used to retrieve the PSSM-ids from best specific/non-specific hits covering >50 % of the protein.

10.6084/m9.figshare.20454691

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Evolutionary pathways for deep-sea adaptation in marine planktonic Actinobacteriota

Frontiers in Microbiology (2023)

Juan J. Roda-García José M. Haro-Moreno Mario López‐Pérez

The deep ocean, one of the largest ecosystems on earth, is dominated by microorganisms that are keystones in the regulation of biogeochemical cycles. However, the evolutionary pathways underlying the specific adaptations required (e.g., high pressure and low temperature) by this unique niche remain understudied. Here, we analyzed the first representatives belonging to the order Acidimicrobiales , a group of marine planktonic Actinobacteriota , that specifically inhabits the aphotic zone of the oceanic water column (>200 m). Compared with their epipelagic counterparts, deep-sea representatives showed the same evolution in genome architecture with higher GC content, longer intergenic spaces as well as higher nitrogen (N-ARSC) and lower carbon (C-ARSC) content in encoded amino acid residue side chains consistent with the higher nitrogen concentration and lower carbon concentration in deep waters compared to the photic zone. Metagenomic recruitment showed distribution patterns that allowed the description of different ecogenomic units within the three deep water-associated genera defined by our phylogenomic analyses (UBA3125, S20-B6 and UBA9410). The entire genus UBA3125 was found exclusively associated with oxygen minimum zones linked to the acquisition of genes involved in denitrification. Genomospecies of genus S20-B6 recruited in samples from both mesopelagic (200–1,000 m) and bathypelagic (1000–4,000 m) zones, including polar regions. Diversity in the genus UBA9410 was higher, with genomospecies widely distributed in temperate zones, others in polar regions, and the only genomospecies associated with abyssal zones (>4,000 m). At the functional level, groups beyond the epipelagic zone have a more complex transcriptional regulation including in their genomes a unique WhiB paralog. In addition, they showed higher metabolic potential for organic carbon and carbohydrate degradation as well as the ability to accumulate glycogen as a source of carbon and energy. This could compensate for energy metabolism in the absence of rhodopsins, which is only present in genomes associated with the photic zone. The abundance in deep samples of cytochrome P450 monooxygenases associated with the genomes of this order suggests an important role in remineralization of recalcitrant compounds throughout the water column.

Mesopelagic zone

Bathyal zone

Oxygen minimum zone

10.3389/fmicb.2023.1159270

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The microbiome of the Black Sea water column analyzed by shotgun and genome centric metagenomics

Environmental Microbiome (2021)

Pedro J. Cabello‐Yeves Cristiana Callieri Antonio Picazo Maliheh Mehrshad José M. Haro-Moreno

Abstract Background The Black Sea is the largest brackish water body in the world, although it is connected to the Mediterranean Sea and presents an upper water layer similar to some regions of the former, albeit with lower salinity and temperature. Despite its well-known hydrology and physicochemical features, this enormous water mass remains poorly studied at the microbial genomics level. Results We have sampled its different water masses and analyzed the microbiome by shotgun and genome-resolved metagenomics, generating a large number of metagenome-assembled genomes (MAGs) from them. We found various similarities with previously described Black Sea metagenomic datasets, that show remarkable stability in its microbiome. Our datasets are also comparable to other marine anoxic water columns like the Cariaco Basin. The oxic zone resembles to standard marine (e.g. Mediterranean) photic zones, with Cyanobacteria ( Synechococcus but a conspicuously absent Prochlorococcus ), and photoheterotrophs domination (largely again with marine relatives). The chemocline presents very different characteristics from the oxic surface with many examples of chemolithotrophic metabolism ( Thioglobus ) and facultatively anaerobic microbes. The euxinic anaerobic zone presents, as expected, features in common with the bottom of meromictic lakes with a massive dominance of sulfate reduction as energy-generating metabolism, a few (but detectable) methanogenesis marker genes, and a large number of “dark matter” streamlined genomes of largely unpredictable ecology. Conclusions The Black Sea oxic zone presents many similarities to the global ocean while the redoxcline and euxinic water masses have similarities to other similar aquatic environments of marine (Cariaco Basin or other Black Sea regions) or freshwater (meromictic monimolimnion strata) origin. The MAG collection represents very well the different types of metabolisms expected in this kind of environment. We are adding critical information about this unique and important ecosystem and its microbiome.

Chemocline

Prochlorococcus

Dominance (genetics)

10.1186/s40793-021-00374-1

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Citations (46)

Nature Communications (2023)

Rafael Gonzalez-Serrano Riccardo Rosselli Juan J. Roda-García Ana-Belén Martín-Cuadrado Francisco Rodríguez‐Valera

The host recognition modules encoding the injection machinery and receptor binding proteins (RBPs) of bacteriophages are predisposed to mutation and recombination to maintain infectivity towards co-evolving bacterial hosts. In this study, we reveal how Alteromonas mediterranea schitovirus A5 shares its host recognition module, including tail fiber and cognate chaperone, with phages from distantly related families including Alteromonas myovirus V22. While the V22 chaperone is essential for producing active tail fibers, here we demonstrate production of functional A5 tail fibers regardless of chaperone co-expression. AlphaFold-generated models of tail fiber and chaperone pairs from phages A5, V22, and other Alteromonas phages reveal how amino acid insertions within both A5-like proteins results in a knob domain duplication in the tail fiber and a chaperone β-hairpin "tentacle" extension. These structural modifications are linked to differences in chaperone dependency between the A5 and V22 tail fibers. Structural similarity between the chaperones and intramolecular chaperone domains of other phage RBPs suggests an additional function of these chaperones as transient fiber "caps". Finally, our identification of homologous host recognition modules from morphologically distinct phages implies that horizontal gene transfer and recombination events between unrelated phages may be a more common process than previously thought among Caudoviricetes phages.

Chaperone (clinical)

Alteromonas

10.1038/s41467-023-42114-8

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Citations (9)