# FirmiData: a set of 40 genomes of Firmicutes with a curated annotation of ICEs and IMEs

Gérard Guédon, Julie Lao, Sophie Payot, Thomas Lacroix, Hélène Chiapello,
Nathalie Leblond-Bourget

► To cite this version:

Gérard Guédon, Julie Lao, Sophie Payot, Thomas Lacroix, Hélène Chiapello, et al. FirmiData: a set of 40 genomes of Firmicutes with a curated annotation of ICEs and IMEs. BMC Research Notes, 2022, 15 (1), pp.157. 10.1186/s13104-022-06036-w. http://hal-03971919

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# FirmiData: a set of 40 genomes of Firmicutes with a curated annotation of ICEs and IMEs

Gérard Guédon<fnref n="1" />, Julie Lao<fnref n="1" />,², Sophie Payot<fnref n="1" />, Thomas Lacroix², Hélène Chiapello² and Nathalie Leblond-Bourget<fnref n="1" />*

## Abstract

**Objectives:** ‘Integrative and Conjugative Elements’ (ICEs) and ‘Integrative and Mobilizable Elements’ (IMEs) are two classes of mobile genetic elements that are complex to detect and delineate. Therefore, they are yet poorly annotated in bacterial genomes. FirmiData provides to the scientific community of microbiologists and bioinformaticians a reference resource of annotated ICEs and of IMEs from Firmicutes. It illustrates their prevalence and their diversity but also gives information on their organization.

FirmiData was designed to assist the scientific community in identifying and annotating these elements by using the sequences of these ICEs and IMEs for the identification of related elements in other genomes of Firmicutes. Therefore, Firmidata meets the needs of the scientific community.

**Data description:** Firmidata provides a manually curated annotation of 98 ICEs and 148 IMEs identified in 40 chromosomes of Firmicutes. The delineation at the nucleotide level of almost all of these elements allows for the characterization of the genes they carry.

**Keywords:** Integrative and conjugative element, Integrative and mobilizable element, Mobile element, Conjugation

## Objective

Unlike conjugative or mobilizable plasmids, ICEs and IMEs are difficult to detect because of their integration into replicons. This is why they have been neglected and even completely ignored for a long time.

However, efforts were made in the last 10 years to develop semi-manual [1, 2] and automatic [3–5] methods to search for conjugative elements in bacterial genomes. These led to the identification of an increasing number of ICEs and IMEs and to the demonstration of their diversity. We currently know that these elements are highly widespread in bacteria and archaea [6–8].

Despite these recent efforts, ICE and IME annotation is very rarely performed and released in public genome

databases. The poor annotation of ICEs and IMEs within bacterial genomes is multifactorial. It results both from the extreme variability of their gene content and from the low specificity of their signature proteins. It is also due to their complex organization since they often form composite elements, with ICEs/IMEs nested within each other and/or organized in tandems.

The objective of FirmiData is to offer to both the communities of microbiologists and bioinformaticians a semi-manual annotation of a large dataset of ICEs and IMEs from Firmicutes. In this work, an expert analysis was done to verify, to characterize and to delimit all ICEs and IMEs they carry. The chromosomes of diverse groups of Firmicutes were chosen to illustrate the diversity of the elements as well as of their various organization into composite elements. The sequences of these elements can be used as reference for the identification of related elements in other genomes of Firmicutes.

<footnote>*Correspondence: nathalie.leblond@univ-lorraine.fr</footnote>

<footnote n="1">¹ DynAMic, Université de Lorraine, INRAE, 54000 Nancy, France
Full list of author information is available at the end of the article</footnote>
## Data description

FirmiData is a set of 40 public annotated genomes of Firmicutes (information on strains are available in Table 1, 'Data file 41', [9]). These genomes were extracted from the Refseq database for which ICEs and IMEs annotation was

added using the standard annotation features and qualifiers used in the Genbank format [9].

The search for ICEs and IMEs relies on data from the literature and on a semi-automated procedure that was described in [1] and [2]. All annotations were carefully

<table><caption>**Table 1** Data sets</caption><thead><tr><td>Label</td><td>Name of data file</td><td>File types</td><td>Data repository and identifier</td></tr></thead><tbody><tr><td>Data file 1</td><td>Cdi630 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 2</td><td>CdiR20291 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 3</td><td>DfoDMC gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 4</td><td>EfalV583 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 5</td><td>EfmISMMSVRE1 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 6</td><td>FprA2-165 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 7</td><td>Lca919 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 8</td><td>LlalO-1 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 9</td><td>LmoLCC2378 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 10</td><td>Lph3177T gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 11</td><td>LspYL32 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 12</td><td>RhoA2-183 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 13</td><td>Sag018883 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 14</td><td>Sag201008 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 15</td><td>SagNEM316 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 16</td><td>SanC1051 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 17</td><td>ScoC1050 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 18</td><td>ScoC232 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 19</td><td>Sdy12394 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 20</td><td>SdyRE378 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 21</td><td>Seq10565 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 22</td><td>Seq35246 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 23</td><td>Sga2069 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 24</td><td>Sparas15912 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 25</td><td>Spn034183 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 26</td><td>SpnP1031 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 27</td><td>Spy2096 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 28</td><td>SpyHKU gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 29</td><td>SsaFDA259 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 30</td><td>Ssal25975 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 31</td><td>SsalJF gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 32</td><td>SsuBM407 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 33</td><td>SsuNSUI002 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 34</td><td>SsuSC84 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 35</td><td>SsuST1 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 36</td><td>SsuT15 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 37</td><td>SsuZYH33 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 38</td><td>Step12228 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 39</td><td>SthJIM8232 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 40</td><td>StpsHKU10-03 gb</td><td>GenBank (gb)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr><tr><td>Data file 41</td><td>Table 1.xlsx</td><td>Excel (xlsx)</td><td>Data INRAE, https://doi.org/10.15454/VI7YRB [9]</td></tr></tbody></table>
checked and corrected when necessary and almost all of
these elements were delineated at the nucleotide level.

ICE expert annotation is based on the identification of
genes carried by their conjugation module and encod-
ing three proteins (relaxase, coupling protein and VirB4)
needed for their transfer. ICE identification also relies
on the search of three types of integrases (tyrosine inte-
grases, serine integrases, and DDE transposases of the
ISLre2 family). IME characterization was done in a simi-
lar fashion as for ICEs except that we searched for genes
carried by their mobilization modules encoding a relax-
ase and eventually a coupling protein.

The co-localization of the genes encoding the signature
proteins attests for the presence of an ICE or an IME.
Their boundaries were then searched. One relevant infor-
mation for the ICE/IME delineation is the knowledge of
the insertion site targeted by their integrase. To get this
information, phylogenetic analyses were done to iden-
tify the closest integrase for which the integration site
was already identified. ICE/IME boundaries were identi-
fied manually by the search for the Direct Repeats (DRs)
flanking the elements. When the DRs were missing, too
short or too degenerated to be detected, the region con-
taining the element was compared with (i) target regions
or genes lacking elements, or (ii) already known and well-
delineated elements.

When an expected signature gene was not identi-
fied within an element, a thorough examination of all its
genes and sequences was done to identify those encoding
the missing signature proteins.

Results

A total of 98 ICEs and 148 IMEs were annotated. We
consider as ICEs the elements that were delimited and
that encode a relaxase, a coupling protein, a VirB4, and
one to three integrases. IMEs are delimited elements that
encode one or two relaxases and eventually a coupling
protein, both distantly related or unrelated to those of
ICES. We also annotated slightly decayed ICEs and IMEs.

The name of the elements indicates (i) their type (ICE or IME), (ii) the strain of the host bacteria and (iii) the target gene. Elements marked with an asterisk are not integrated in their primary site but in a secondary one. Those marked with “unk” are integrated in a gene of unknown function. The site of insertion of those labeled with ND or NS is non-determined and non-specific, respectively.

In conclusion, the FirmiData dataset constitutes a
valuable resource for (i) the microbiologist community
interested in mobile genetic elements annotation (ii) the
bioinformatics teams developing annotation tools and
strategies to detect and annotate mobile genetic elements
in bacterial genomes.

Limitations

* Isolate genes encoding a signature protein or too decayed ICEs or IMEs were not taken into consideration.

* Elements encoding an integrase but devoid of relaxase were not annotated.

Abbreviations

ICE: Integrative and conjugative element; IME: Integrative and mobilizable element; DRs: Direct repeats.

Acknowledgements

Not applicable

Author contributions

GG: formal analysis, writing—review & editing; SP: formal analysis, writing—review & editing; JL: production of the new annotated Genbank files, writing—review & editing; TL: writing—review & editing; HC: funding acquisition, writing—review & editing; NLB: production of the new annotated Genbank files, funding acquisition, writing—original draft. All authors read and approved the final manuscript.

Funding

This work was supported by the Université de Lorraine, the Région Grand-
Est and INRAE. This work was co-funded by the french PIA project "Lorraine
Université d'Excellence" (ANR-15-IDEX-04-LUE), and by the European Union
through the Regional Operational Program of the European Regional Devel-
opment Fund (ERDF).

Availability of data and materials

The data described in this Data note can be freely and openly accessed on
Data INRAE (https://doi.org/10.15454/VI7YRB). Please see Table 1 and reference
[9] for details and links to the data.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

The authors declare that they all consent for publication.

Competing interests

The authors declare that they have no competing interests.

Author details

¹DynAMic, Université de Lorraine, INRAE, 54000 Nancy, France. ²MalAGE,
Université Paris-Saclay, INRAE, 78350 Jouy-en-Josas, France.

Received: 16 December 2021 Accepted: 11 April 2022

Published online: 10 May 2022

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