A curated database of cyanobacterial strains relevant for modern taxonomy and phylogenetic studies

Abstract

The dataset herein described lays the groundwork for an online database of relevant cyanobacterial strains, named CyanoType (http://lege.ciimar.up.pt/cyanotype). It is a database that includes categorized cyanobacterial strains useful for taxonomic, phylogenetic or genomic purposes, with associated information obtained by means of a literature-based curation. The dataset lists 371 strains and represents the first version of the database (CyanoType v.1). Information for each strain includes strain synonymy and/or co-identity, strain categorization, habitat, accession numbers for molecular data, taxonomy and nomenclature notes according to three different classification schemes, hierarchical automatic classification, phylogenetic placement according to a selection of relevant studies (including this), and important bibliographic references. The database will be updated periodically, namely by adding new strains meeting the criteria for inclusion and by revising and adding up-to-date metadata for strains already listed. A global 16S rDNA-based phylogeny is provided in order to assist users when choosing the appropriate strains for their studies.

OPEN

Data Descriptor: A curated database of cyanobacterial strains relevant for modern taxonomy and phylogenetic studies

Received: 22 June 2016

Accepted: 20 March 2017

Published: 25 April 2017

Vitor Ramos1,2, Joo Morais1 & Vitor M. Vasconcelos1,2

The dataset herein described lays the groundwork for an online database of relevant cyanobacterial strains, named CyanoType (http://lege.ciimar.up.pt/cyanotype

Web End =http://lege.ciimar.up.pt/cyanotype). It is a database that includes categorized cyanobacterial strains useful for taxonomic, phylogenetic or genomic purposes, with associated information obtained by means of a literature-based curation. The dataset lists 371 strains and represents the rst version of the database (CyanoType v.1). Information for each strain includes strain synonymy and/or co-identity, strain categorization, habitat, accession numbers for molecular data, taxonomy and nomenclature notes according to three different classication schemes, hierarchical automatic classication, phylogenetic placement according to a selection of relevant studies (including this), and important bibliographic references. The database will be updated periodically, namely by adding new strains meeting the criteria for inclusion and by revising and adding up-to-date metadata for strains already listed. A global 16S rDNA-based phylogeny is provided in order to assist users when choosing the appropriate strains for their studies.

data integration objective database creation objective species comparison

design sequence-based phylogenetic analysis objective

Measurement Type(s) computational phylogenetic analysis

Technology Type(s) digital curation

Factor Type(s) organism subspecies

Sample Characteristic(s) Cyanobacteria

1CIIMAR/CIMARInterdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de

Cruzeiros do Porto de Leixes, Av. General Norton de Matos s/n, Matosinhos 4450-208, Portugal. 2Faculdade de

Cincias, Universidade do Porto, Rua do Campo Alegre, Porto 4169-007, Portugal. Correspondence and requests

for materials should be addressed to V.M.V. (email: mailto:[email protected]

Web End [email protected] ).

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Design Type(s)

Background & Summary

Strains held in culture collections are pivotal for comparative purposes in current taxonomic or phylogenetic studies of prokaryotes in general, and cyanobacteria in particular. In recent years, the number of new cyanobacterial genera established by a modern polyphasic taxonomy (i.e., following a combination of different techniques) has greatly increased1, resulting in the designation of several new Type strains (i.e., an isolate based on which the author describes a new species or genus; it is often the holotype specimen itself).

Concerning nomenclature, cyanobacteria (formerly known as blue-green algae) are a special case among the prokaryotes, since they are ruled either by the International Code of Nomenclature for algae, fungi, and plants (ICN; formerly the International Code of Botanical Nomenclature, ICBN) or by the International Code of Nomenclature of Prokaryotes (ICNP, formerly the International Code of Nomenclature of Bacteria, ICNB). Nomenclature rules governed by these two entities are converging15

but due to this duality two general types of systematics still exists: the more ancient botanical/ phycological classication scheme and the bacteriological scheme4. Available keys for the identication of cyanobacteria are mostly based on the botanical system proposed by Geitler in 1932 (ref. 6), including the key present in the pioneering bacteriological system of Stanier and colleagues2,7. One important

classication system followed by microbiologists is the Bergeys Manual of Systematic Bacteriology, often confused as an ofcial classication, which is not the case8. The manual classies the cyanobacteria in form genera which, in turn, are divided into clusters or subclusters9. For each (sub)cluster at least one Reference strain is assigned. This strain category, as presented in the manual, should not be confused with being a Type strain (though some of them effectively are). Moreover, the term form genus has no standing under the Bacteriological or under the Botanical Codes of Nomenclature2 and the authors of the cyanobacterial section of the manual early admitted that the proposed classication is a temporary one2,9.

Despite these taxonomic issues, the Bergeys Manual is an important body of work, since it systematizes, lists and characterizes a good number of cyanobacterial strains, most of which are widely used as reference in phylogenetic studies.

Several new taxa that have been recently established emerge from taxonomic revisions of classical botanical genera, which have been described primarily by their morphological features. Most of them are in fact polyphyletic, as depicted from 16S rRNA gene-based phylogenies using strains assigned to different species of such genera1,4,9. Since the pioneering work of Carl Woese, George Fox and colleagues1012, the 16S rRNA gene became, and still is, the most important and widely used molecular marker for the identication of prokaryotes. However, its resolving power at species level is low13, and

should therefore be employed to obtain identications at the genus level. Nonetheless, its appropriateness for phylogenetic-based classications was again demonstrated more recently. Shih et al.14 have

demonstrated, following a phylogenomic approach involving 54 cyanobacterial genomes, that the 16S rRNA phylogeny is highly congruent with that obtained from a concatenation of 31 conserved proteins. Thus, it is likely that the 16S rRNA gene will continue to be the standard molecular marker for proposing new cyanobacterial genera1. The emergence of genome-based taxonomy15 approaches, however, renders genome-sequenced strains increasingly important to the eld.

Due to the above-mentioned issues, choosing the proper strains to include in taxonomic, phylogenetic or comparative genomic studies on cyanobacteria is very often a challenging task. In order to overcome this difculty, we introduce the curated dataset of CyanoType v.1, a database with an extensive list of relevant cyanobacterial strains classied by importance category, i.e., with the indication about being a Type strain, a Reference strain sensu Bergeys Manual, and/or a strain having its genome sequenced. The dataset encompasses different types of metadata (e.g., strain synonymy and/or co-identity), including a reference list for each strain. In order to help users in their process of selecting strains, we provide two 16S rDNA-based phylogenetic trees for guidance. The main phylogenetic tree and the information for each strain included in the dataset is available in the searchable, online database at http://lege.ciimar.up.pt/cyanotype

Web End =http://lege.ciimar.up. http://lege.ciimar.up.pt/cyanotype

Web End =pt/cyanotype .

Methods

Figure 1 illustrates the workow followed for the literature and database searches performed in this study.

Data acquisition

We initially established the criteria for inclusion of cyanobacterial strains in the dataset. We have considered three main groups of strains to be included, representing different levels of importance from the taxonomic point of view: (1) strains that were used as Type strains for the proposal or establishment of a new taxon by mean of a modern, polyphasic taxonomic approach1, (2) strains that are included as Reference strains in Bergey's Manual of Systematic Bacteriology9, and (3) strains that have their genome sequenced and publicly available. Following these criteria, and through literature and online database searches, we have obtained a list of relevant strains categorized by taxonomic importance.

Literature searches for Type strains were rstly guided by information included in the work of Komrek et al.1, which lists the cyanobacterial genera for which the holotype (i.e., Type species) was described using a modern, polyphasic taxonomic approach. To avoid missing any Type strain (e.g., strains from new genera arising from later studies than those included in Komrek et al.1) we have

performed complementary searches in literature databases such as ISI Web of Science, Scopus, PubMed

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Figure 1. Diagram illustrating the workow followed during the construction and release of the dataset (standard owchart symbols were used).

and Google Scholar using the following Boolean search string: ((cyanobact* OR cyanophy*) AND ((gen. nov. OR gen. et sp. nov.) OR new genus OR novel genus OR new genera OR novel genera) for the elds [Title, Abstract, Keywords]. Duplicate articles were eliminated. We then fully examined the search results to evaluate the suitability of the articles for our research.

The dataset also includes Reference strains from all clusters or subclusters dened in the Bergeys Manual9, and known relatives (as indicated in the Manual) if the 16S rRNA gene sequences for the Reference strains were not available. The number of strains tting in each category are summarized in Table 1. A full description of each category type can be found in the Data Records section (see Strain_Category). We have alsoas was done for strainsperformed literature and online database searches for data and metadata acquisition. For instance, we manually performed data mining in public molecular (e.g., NCBI) and taxonomic (e.g., AlgaeBase, http://www.algaebase.org/

Web End =http://www.algaebase.org/ ) databases and searches on websites of Culture Collections.

Finally, strains with available cyanobacterial genomes were also included in the dataset. The work of Shih et al.14 was used as a reference rst list. To obtain the full list, we have then used the Assembly database and other NCBI resources (e.g., Genome, Genome BLAST, BLASTn) in order to search for genomes and to obtain accession numbers and 16S rRNA gene nucleotide sequences from the strains. The search term Cyanobacteria (Taxonomy ID: 1,117) was used to obtain the list of available cyanobacterial genomes. For our study, we have considered 251 out of 372 strains having their genomes available in NCBI (until the end of 2015). Missing strains are Prochlorococcus spp. which were not included in the dataset due to overrepresentation and phylogenetic redundancy. Even so, the dataset comprises 28 representatives, by far the most represented genus (Data Citation 1).

All strains with available 16S rRNA gene nucleotide sequences were then subjected to a phylogenetic study (see Subsection Phylogenetic analyses below). First, in order to obtain the sequences, we have performed Boolean searches in the NCBI Nucleotide database (which includes GenBank). For some strains it was necessary to extract the sequences by mining their genome. Accession numbers were recorded in the dataset (Data Citation 1). Adequacy of the sequences length for multiple alignment and further analyses was then checked (see Subsection Phylogenetic analyses). Additionally, the 16S rRNA gene sequences were submitted to the automatic RDP Naive Bayesian rRNA Classier v2.6 (ref. 16) pipeline. Strains were ranked and the hierarchical classication result recorded (Data Citation 1).

Moreover, we have classied the strains at higher taxonomic levels (Order and Family) and veried the nomenclatural status of taxon names according to taxonomic concepts followed in Komarek et al.1 (at the Genus level), and in AlgaeBase (Species level), and recorded it in the dataset (Data Citation 1). The same was made to other names by which the strain may be known or to conicting identications of

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Strain category* # of strains # of strains included in the provided phylogenetic trees T or t, only 73 63T or t and R or r 5 4T or t and G 10 10T or t and R or r and G 9 9R or r and G 60 60R or r, only 41 30G, only 172 155E 1 1TOTAL 371 332

Table 1. Number of cyanobacterial strains included in version 1 of the CyanoType dataset and present in the phylogenetic trees obtained in this study, by category: T, Type strain of the Type species; t, not the type strain, but phylogenetically close-related; R, Reference strain in Bergey's Manual of Systematic Bacteriology9; r, not the reference strain, but phylogenetically close-related; G, strain with its genome sequenced and publicly available; E, strain studied from exsiccata. *see also categories descriptions in the Data Records section.

co-identical strains. Whenever relevant, we have also added additional taxonomy or nomenclature notes/clarications to the dataset (e.g., indication of whether it is the Type strain of the holotype).

Phylogenetic analyses

All bioinformatics procedures and analyses were conducted using the MEGA7 software package17.

Sequences were aligned using the ClustalW algorithm. Strains with small-sized sequences (o1,000 nt) were treated separately, to avoid reducing the number of unambiguously aligned nucleotide positions, and thus preventing distortion of the main phylogeny. Molecular phylogenetic analyses were inferred by using the Maximum Likelihood (ML) method, based on the nucleotide substitution model that best t the alignment data. By applying the corrected Akaikes Information Criterion (AICc), the chosen nucleotide substitution model was General Time Reversible (GTR) for both analyses. A discrete Gamma distribution ([+G]) was used to model evolutionary rate differences among sites, while the rate variation model allowed for some sites to be evolutionarily invariable ([+I]). The trees with the highest log likelihood (27524.3318 and 7982.8912, respectively) are shown for the main (Supplementary Fig. 1) and complementary (Fig. 2) phylogenies. Both trees were rooted with the outgroup Chloroexus aurantiacus J-10- (NR_074263).

The phylogenetic analysis for the main tree (Supplementary Fig. 1) involved 333 nucleotide sequences. This gure is available online only. All positions containing gaps and missing data were eliminated. The nal alignment dataset consisted of 863 positions. In order to systematize the phylogenetic placement of the cyanobacterial strains, we have grouped the strains into clusters (broader groups; for sequences placed together but lacking bootstrap support) and in clades (for groups of sequences with a ML bootstrap support), as depicted in Supplementary Fig. 1. This primary data was included in the dataset (see also Phylog_This_Work, in the Data Records section). We have also described the phylogenetic placement of the strains according to a selection of important studies1823 (Data Citation 1).

In turn, the analysis performed for the complementary phylogenetic tree (Fig. 2) involved 67 nucleotide sequences. This tree is meant to show the placement of those shorter sequences that were not included in the main tree (six sequences, ranging from 381 to 898 nt; three strains with sequences o315 nt were discarded from the analysis). To do so, we have also included 60 cyanobacterial sequences used in the main tree. The selection of strains involved representatives from all the clades identied in Supplementary Fig. 1 (for larger clades, we have selected a number of divergent strains), intending to cover the cyanobacterial diversity contained in CyanoType v.1. Due to the inclusion of short sequences, less than 5% gaps, missing data, and ambiguous bases were allowed at any position of the alignment. This resulted in a total of 533 positions in the nal alignment.

The survey and collection of the different data or metadata (including important bibliographic references for each strain) was nished by the end of 2015, for this version of the database (Data Citation 1).

Data Records

The dataset, the sequence alignments and the tree les (Data Citation 1) obtained in this work are deposited at FigShare.

The dataset (CyanoType_data_v1.0.csv) is a semi-comma separated values le containing taxonomic-and phylogenetic-related data and other useful information for each cyanobacterial strain considered in this work, including important strain-related references when available (e.g., literature for strain origin,

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Figure 2. Example of the use of the proposed subset of strains representing the cyanobacterial tree of life (see Subset_Condens_Tree in the Data Records section and Phylogenetic analyses in Methods) to evaluate the phylogenetic placement of strains not included in Supplementary Fig. 1 due to having short 16S rRNA gene sequences (in bold). The evolutionary history was inferred by using the Maximum Likelihood method based on the GTR+G+I model. Bootstrap values indicated near internal branches; values below 50% were omitted. Information for each cyanobacterial strain include accession number of the nucleotide sequence, strain ID, eventual taxonomic synonyms or other strain names (in parentheses), and co-identical strains or other strain codes (in parentheses). Letters after colon indicate the categorization of strains as follows (see also Strain_Category in Data Record section): T, Type strain of the Type species; t, not the type strain, but phylogenetically close-related; R, Reference strain in Bergey's Manual of Systematic Bacteriology9; r, not the reference strain, but phylogenetically close-related; G, strain with its genome sequenced and publicly available; E, strain studied from exsiccata. A letter in parentheses means that there is a taxonomic-related uncertainty with the taxon name (see taxonomic comments) or the assigned strains category couldnt be yet fully conrmed (e.g., for provisional species names). The outgroup was pruned from the tree for clarity. The scale bar represents nucleotide substitutions per site.

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identication/characterization, taxonomy, phylogeny and/or genome sequencing). Rows represent single strains, for which data were integrated. Columns are for useful information and metadata, as follow:

Entry_number

It is the entry number of the cyanobacterial strain in the dataset.

Strain_ID

Taxon name and strain code.

Strain_Other_ID

Other taxon name(s) previously assigned to the strain, synonym(s) of the taxon name, or other putative taxonomic designation(s).

Strain_Co-Ident

Older code(s) for the strain, misspellings or code(s) from co-identical strains (e.g., same strain deposited in other(s) culture collection(s); not an exhaustive list).

Strain_Category

Categorization of strains by relevance, as dened in this work, and additional important strain characterization. T, Type strain of the Type species (taxon established by modern polyphasic taxonomy); t, not the type strain but known to have the same phylogenetic placement as the Type species, after taxonomic revision; R, Reference strain in Bergey's Manual of Systematic Bacteriology9; r, strain known to be included in the same phylogenetic cluster as the reference strain, as mentioned in the Bergey's Manual9 ; G, strain with its Genome sequenced and publicly available; E, strain studied from Exsiccata (dried herbarium specimens of cyanobacteria). A letter in parentheses means that there is a taxonomic-related uncertainty with the taxon name (see taxonomic comments) or the assigned strains category could not be satisfactorily conrmed (e.g., for unpublished, provisional species names).

Strain_Addition

Additional characterization of the strain concerning its isolation status. Co-culture is for strains in culture but associated with other organism (i.e., not free-living isolates).

Environment

Type of environment from which the strain was obtained.

Habitat_notes

Additional details on the source/origin or lifestyle of the strain.

16S_Acc_Nbr

GenBank accession number for the 16S rRNA gene sequence.

NCBI_ID

NCBI Assembly or BioProject numbers for available cyanobacterial genomes.

Tax_Komarek_Ord_Fam

Order and family assignments for the strain identication(s), according to the recent classication scheme proposed by Komrek et al.1

Tax_Status_Genus

Status of the genus as depicted from Appendix 1 in Komrek et al.1, as follows: 1genera supported by a molecular phylogeny, including a 16S rRNA gene sequence of the type species; 2genera, from which only one or a few species were studied using molecular methods and for which there is no 16S rRNA gene data for the type species; 3genera studied using molecular methods and found to be poly/paraphyletic or with no clear relationship with other genera; 4genera not yet studied using molecular methods; 5genera not yet validly described; 16S-Typegenera for which there is a 16S rRNA sequence for the type material publicly available (in parentheses, when this availability is not indicated in Komrek et al.1);

problematic genera from the taxonomic point of view.

Tax_AlgaeBase_Ord_Fam

Order and family assignments for the strain identication(s), according to the online database AlgaeBase (http://www.algaebase.org/

Web End =http://www.algaebase.org/).

Tax_Status_AlgaeBase_&_Tax_Notes

Status of the strains taxon name as present in AlgaeBase (http://www.algaebase.org/

Web End =http://www.algaebase.org/). When applicable, we indicate whether it is a type strain (i.e., holotype or epitype). It might also include other primary data, such as taxonomic relevant comments or notes.

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Tax_AlgaeBase_Holotype

Type species of the genus (holotype) and authority as indicated in AlgaeBase (http://www.algaebase.org/

Web End =http://www.algaebase.org/). It may include some additional taxonomic relevant comments or notes.

Tax_Bergey's

Classication according to the Bergey's Manual scheme9, in condensed form. The rst roman numerals refer to subsections, while the second refer to form-genus within that subsection.

Phylog_This_Work

Position of the strain within the phylogenetic tree illustrated in Supplementary Fig. 1 (capital letters and numbers refer to clusters and clades, respectively).

Subset_Condens_Tree

Subset of 60 strains for a proposal of a condensed phylogenetic tree covering the cyanobacterial diversity included in CyanoType (see also Fig. 2 and the Subsection Phylogenetic analyses in Methods). The goal of this suggested subset is to aid users in preliminary phylogenetic analyses, namely to discern the placement of their sequences in relation to relevant strains.

Phylog_RDP_Classier

Classication according to the automatic RDP Naive Bayesian rRNA Classier16.

Phylog_Shih

Phylogenetic placement of the strain (clade or sub-clade) as established in Shih et al.14

Phylog_Howard-Azzeh

Phylogenetic placement of the strain (clade or sub-clade) as established in Howard-Azzeh et al.19

Phylog_Schirrmeister

Phylogenetic placement of the strain (clade or sub-clade) as established in Schirrmeister et al.19

Phylog_Picocyano

Ecotypes as established or present in Ahlgren & Rocap20, Ahlgren et al.21, Kettler et al.22 or Scanlan et al.23. For Prochlorococcus and Synechococcus spp. strains only.

Metadata_Shih

Information for additional metadata present in Shih et al.14.

References

Important literature related with the strain (e.g., with information on isolation/source origin, identication/taxonomy, phylogeny, genome sequencing, etc.).

Technical Validation

The dataset was extensively checked for double entries, errors or inconsistencies (all elds), while data or metadata concerning each entry (i.e., strain) was further revised, very particularly decisions about category attribution (see Fig. 1). Whenever available, bibliographic references are provided for each entry, enabling any user to get access to the original data. Researchers making use of the dataset (Data Citation 1) or the database are encouraged to assess the validity and accuracy of the data and send us feedback through the website database, at http://lege.ciimar.up.pt/cyanotype

Web End =http://lege.ciimar.up.pt/cyanotype . The information will be updated after curation by our team.

In the future, it is intended that the information for any given entry (i.e., strain) in the database may be curated on a voluntary basis. To this end, administrative and managerial procedures for quality control of data will be implemented. For instance, users will need to request permission to become a contributor and will have a user account. Any observation made by a contributor will be agged and simultaneously an automatic message will be sent to the administrator. The pending ag will be removed only after administrator approval. The observation made by the contributor for a particular strain will be then recorded and become accessible to other users, as updated information for that strain.

References

1. Komrek, J., Katovsk, J., Mare, J. & Johansen, J. R. Taxonomic classication of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86, 295335 (2014).

2. Oren, A. A proposal for further integration of the cyanobacteria under the Bacteriological Code. Int. J. Syst. Evol. Microbiol. 54, 18951902 (2004).

3. Oren, A. Cyanobacterial systematics and nomenclature as featured in the International Bulletin of Bacteriological Nomenclature and Taxonomy/International Journal of Systematic Bacteriology/International Journal of Systematic and Evolutionary Microbiology. Int. J. Syst. Evol. Microbiol. 61, 1015 (2011).

4. Palinska, K. A. & Surosz, W. Taxonomy of cyanobacteria: a contribution to consensus approach. Hydrobiologia 740, 111 (2014).5. Pinevich, A. V. Proposal to consistently apply the International Code of Nomenclature of Prokaryotes (ICNP) to names of the oxygenic photosynthetic bacteria (cyanobacteria), including those validly published under the International Code of Botanical

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Nomenclature (ICBN)/International Code of Nomenclature for algae, fungi and plants (ICN), and proposal to change Principle 2 of the ICNP. Int. J. Syst. Evol. Microbiol. 65, 10701074 (2015).6. Geitler, L. in Dr L Rabenhorsts Kryptogamen-Flora von Deutschland sterreich und der Schweiz. Vol. 14 Cyanophyceae (Akademische Verlag, 1932).

7. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 161 (1979).

8. Brenner, D. J., Staley, J. T., Krieg, N. R. in Bergey's Manual of Systematic Bacteriology 2nd edn. Vol. 2. The Proteobacteria (ed. Garrity G.) 2732 (Springer, 2005).

9. Boone, D. R. & Castenholz, R. W. Bergey's Manual of Systematic Bacteriology 2nd edn. Vol. 1. The Archaea and the Deeply Branching and Phototrophic Bacteria (Springer-Verlag, 2001).

10. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. USA 74, 50885090 (1977).

11. Fox, G. E., Magrum, L. J., Balch, W. E., Wolfe, R. S. & Woese, C. R. Classication of methanogenic bacteria by 16S ribosomal RNA characterization. Proc. Natl. Acad. Sci. USA 74, 45374541 (1977).

12. Balch, W. E., Magrum, L. J., Fox, G. E., Wolfe, R. S. & Woese, C. R. An ancient divergence among the bacteria. J. Mol. Evol. 9, 305311 (1977).

13. Rossell-Mora, R. & Amann, R. The species concept for prokaryotes. FEMS Microbiol. Rev. 25, 3967 (2001).14. Shih, P. M. et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. USA 110, 10531058 (2013).

15. Konstantinidis, K. T. & Tiedje, J. M. Towards a genome-based taxonomy for prokaryotes. J. Bacteriol. 187, 62586264 (2005).16. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Nave Bayesian classier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 52615267 (2007).

17. Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 18701874 (2016).

18. Howard-Azzeh, M., Shamseer, L., Schellhorn, H. E. & Gupta, R. S. Phylogenetic analysis and molecular signatures dening a monophyletic clade of heterocystous cyanobacteria and identifying its closest relatives. Photosynth. Res. 122, 171185 (2014).

19. Schirrmeister, B. E., Antonelli, A. & Bagheri, H. C. The origin of multicellularity in cyanobacteria. BMC Evol. Biol. 11, 45 (2011).20. Ahlgren, N. A. & Rocap, G. Diversity and distribution of marine Synechococcus: multiple gene phylogenies for consensus classication and development of qPCR assays for sensitive measurement of clades in the ocean. Front. Microbiol. 3, 213 (2012).

21. Ahlgren, N. A., Rocap, G. & Chisholm, S. W. Measurement of Prochlorococcus ecotypes using real-time polymerase chain reaction reveals different abundances of genotypes with similar light physiologies. Environ. Microbiol. 8, 441454 (2006).

22. Kettler, G. C. et al. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet. 3, e231 (2007).23. Scanlan, D. J. et al. Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev. 73, 249299 (2009).

Data Citation

1. Ramos, V. & Vasconcelos, V. Figshare https://doi.org/10.6084/m9.figshare.c.3273731

Web End =https://doi.org/10.6084/m9.gshare.c.3273731 (2017).

Acknowledgements

This work was supported in part by FCTFoundation for Science and Technology under the project UID/Multi/04423/2013 and by the Structured Program of R&D&I INNOVMARInnovation and Sustainability in the Management and Exploitation of Marine Resources (reference NORTE-01-0145-FEDER-000035, Research Line NOVELMAR), funded by the Northern Regional Operational Program (NORTE2020) through the European Regional Development Fund (ERDF). V.R. was supported by the FCT fellowship SFRH/BD/80153/2011.

Author Contributions

V.R. led the project, collected and assembled the data, performed the phylogenetic analysis and prepared the manuscript. J.M. revised the dataset and the manuscript and participated in the construction of the database. V.V. supervised the work and was involved in all stages of data assembly, revised the dataset and the manuscript.

Additional Information

Supplementary Information accompanies this paper at http://www.nature.com/sdata

Web End =http://www.nature.com/sdata

Competing interests: The authors declare no competing nancial interests.

How to cite this article: Ramos, V. et al. A curated database of cyanobacterial strains relevant for modern taxonomy and phylogenetic studies. Sci. Data 4:170054 doi: 10.1038/sdata.2017.54 (2017).

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