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Genomics and phylogeny of the proposed phylum ‘Candidatus Poribacteria’ associated with the excavating sponge Thoosa mismalolli

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Abstract

Members of the proposed phylum ‘Candidatus Poribacteria’ are among the most abundant microorganisms in the highly diverse microbiome of the sponge mesohyl. Genomic and phylogenetic characteristics of this proposed phylum are barely known. In this study, we analyzed metagenome-assembled genomes (MAGs) obtained from the coral reef excavating sponge Thoosa mismalolli from the Mexican Pacific Ocean. Two MAGs were extracted and analyzed together with 32 MAGs and single-amplified genomes (SAGs) obtained from NCBI. The phylogenetic tree based on the sequences of 139 single-copy genes (SCG) showed two clades. Clade A (23 genomes) represented 67.7% of the total of the genomes, while clade B (11 genomes) comprised 32.3% of the genomes. The Average Nucleotide Identity (ANI) showed values between 66 and 99% for the genomes of the proposed phylum, and the pangenome of genomes revealed a total of 37,234 genes that included 1722 core gene. The number of genes used in the phylogenetic analysis increased from 28 (previous studies) to 139 (this study), which allowed a better resolution of the phylogeny of the proposed phylum. The results supported the two previously described classes, ‘Candidatus Entoporibacteria’ and ‘Candidatus Pelagiporibacteria’, and the genomes SB0101 and SB0202 obtained in this study belong to two new species of the class ‘Candidatus Entoporibacteria’. This is the first comparative study that includes MAGs from a non-sponge host (Porites lutea) to elucidate the taxonomy of the poorly known Candidatus phylum in a polyphasic approach. Finally, our study also contributes to the sponge microbiome project by reporting the first MAGs of the proposed phylum ‘Candidatus Poribacteria’ isolated from the excavating sponge T. mismalolli.

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Data availability

The SB0101 and SB0202 genomes have been deposited at DDBJ/EMBL/GenBank under the project accession number (JAGFCB01 for the proposed phylum Candidatus Poribacteria SB0101), and JAGFCA01 for the proposed phylum Candidatus Poribacteria SB0202). The initial descriptions of these genomes are in this paper.

Abbreviations

MAG:

Metagenome-assembled genome

SAG:

Single-amplified genome

ANI:

Average nucleotide identity

MEMs:

Maximum exact matches

PVC:

Planctomycetes, Verrucomicrobia, Chlamydiae

References

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59(1):143–169

    Article  CAS  Google Scholar 

  • Auch AF, von Jan M, Klenk HP, Göker M (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genom Sci 2:117–134

    Article  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75

    Article  Google Scholar 

  • Bautista-Guerrero E, Carballo JL, Aguilar-Camacho JM, Sifuentes-Romero I (2016) Molecular and morphological differentiation of sympatric larvae of coral excavating sponges of genus Thoosa. Zoomorphology 135:159–165

    Article  Google Scholar 

  • Bell JJ (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353

    Article  Google Scholar 

  • Bell JJ, Smith D (2004) Ecology of sponge assemblages (Porifera) in the Wakatobi region, south-east Sulawesi, Indonesia: Richness and abundance. J Mar Biol Assoc UK 84:581–591

    Article  Google Scholar 

  • Campos AB, Cavalcante LC, de Azevedo AR, Loiola M, Silva AET, Ara A, Meirelles PM (2021) CPR and DPANN have an overlooked role in corals’ microbial community structure. Microb Ecol. https://doi.org/10.1007/s00248-021-01737-4

    Article  PubMed  Google Scholar 

  • Chen L-X, Anantharaman K, Shaiber A, Eren AM, Banfield JF (2020) Accurate and complete genomes from metagenomes. Genome Res 30:315–333. https://doi.org/10.1101/gr.258640.119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dayton PK, Mordida BJ, Bacon F (1994) Polar marine communities. Am Zool 34:90–99

    Article  Google Scholar 

  • Engelberts JP, Robbins SJ, de Goeij JM, Aranda M, Bell SC, Webster NS (2020) Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J14:1100–1110. https://doi.org/10.1038/s41396-020-0591-9

    Article  CAS  Google Scholar 

  • Eren AM, Esen OC, Quince C, Vinies JH, Morrison HG, Sogin ML (2015) Anvi’o: an advanced analysis and visualization platform for ‘omics data. Peer J 3:e1319

    Article  Google Scholar 

  • Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum ‘‘Poribacteria’’ in marine sponges. Appl Environ Microb 70:3724–3732

    Article  CAS  Google Scholar 

  • Fieseler L, Quaiser A, Schleper C, Hentschel U (2006) Analysis of the first genome fragment from the marine sponge-associated, novel candidate phylum Poribacteria by environmental genomics. Environ Microbiol 8:612–624

    Article  CAS  Google Scholar 

  • Gloeckner V, Wehrl M, Moitinho-Silva L, Gernert C, Hentschel U, Schupp P, Pawlik JR (2014) The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biol Bull 227:78–88

    Article  Google Scholar 

  • González-Castillo A, Enciso-Ibarra J, Gomez-Gil B (2020) Genomic taxonomy of the Mediterranei clade of the genus Vibrio (Gammaproteobacteria). Antonie Van Leeuwenhoek 113:851–859. https://doi.org/10.1007/s10482-020-01396-4

    Article  CAS  PubMed  Google Scholar 

  • Gutleben J, Chaib De Mares M, van Elsas JD, Smidt H, Overmann J, Sipkema D (2018) The multi-omics promise in context: from sequence to microbial isolate. Crit Rev Microbiol 44(2):212–229. https://doi.org/10.1080/1040841X.2017.1332003

    Article  CAS  PubMed  Google Scholar 

  • Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440

    Article  CAS  Google Scholar 

  • Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10:641–654

    Article  CAS  Google Scholar 

  • Henz S, Huson D, Auch AF, Nieselt-Struwe K, Schuster S (2005) Whole-genome prokaryotic phylogeny. Bioinformatics 21:2329–2335

    Article  CAS  Google Scholar 

  • Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11:119

    Article  Google Scholar 

  • Kamke J, Rinke C, Schwientek P, Mavromatis K, Ivanova N, Sczyrba A, Woyke T, Hentschel U (2014) The candidate phylum Poribacteria by single-cell genomics: new insights into phylogeny, cell-compartmentation, eukaryote-like repeat proteins, and other genomic features. PLoS ONE 9(1):e87353. https://doi.org/10.1371/journal.pone.0087353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller-Costa T, Lago-Lestón A, Saraiva JP, Toscan R, Silva SG, Gonçalves J, Cox CJ, Kyrpides N, da Rocha UN, Costa R (2021) Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals. Microbiome 9:72. https://doi.org/10.1186/s40168-021-01031-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci 102:2567–2572

    Article  CAS  Google Scholar 

  • Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes T, Ussery D (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Meth 9:357–359

    Article  CAS  Google Scholar 

  • Lee STM, Kahn SA, Delmont TO, Shaiber A, Esen ÖC, Hubert NA, Morrison HG, Antonopoulos DA, Rubin DT, Eren AM (2017) Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics. Microbiome 5:50

    Article  Google Scholar 

  • Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K, Yamashita H, Lam TW (2016) MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 102:3–11

    Article  CAS  Google Scholar 

  • Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP, Bradley AS, Kelly AE, Bhatia M, Meredith W, Snape CE, Bowring SA, Condon DJ, Summons RE (2009) Fossil steroids record the appearance of demospongiae during the cryogenian period. Nature 457:718–721

    Article  CAS  Google Scholar 

  • Meier-Kolthoff JP, Alexander AF, Hans-Peter K, Markus K (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60

    Article  Google Scholar 

  • Moitinho-Silva L, Nielsen S, Amir A, Gonzalez A, Ackermann GL, Cerrano C, Astudillo-Garcia C, Easson C, Sipkema D, Liu F, Steinert G, Kotoulas G, McCormack GP, Feng G, Bell JJ, Vicente J, Björk JR, Montoya JM, Olson JB, Reveillaud J, Steindler L, Pineda MC, Marra MV, Ilan M, Taylor MW, Polymenakou P, Erwin PM, Schupp PJ, Simister RL, Knight R, Thacker RW, Costa R, Hill RT, Lopez-Legentil S, Dailianis T, Ravasi T, Hentschel U, Li Z, Webster NS, Thomas T (2017) The sponge microbiome project. Gigascience 6(10):1–7. https://doi.org/10.1093/gigascience/gix077 (Erratum in: Gigascience. 2018 Dec 1; 7(12))

    Article  PubMed  Google Scholar 

  • Podell S, Blanton JM, Neu A, Agarwal V, Biggs JS, Moore BS, Allen EE (2019) Pangenomic comparison of globally distributed Poribacteria associated with sponge hosts and marine particles. ISME J 13:468–481

    Article  CAS  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106:19126–19131

    Article  CAS  Google Scholar 

  • Robbins SJ, Singleton CM, Chan CX, Messer LF, Geers AU, Ying H, Baker A, Bell SC, Morrow KM, Ragan MA, Miller DJ, Forêt S, Voolstra CR, Tyson GW, Bourne DG (2019) A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat Microbiol 4:2090–2100. https://doi.org/10.1038/s41564-019-0532-4

    Article  CAS  PubMed  Google Scholar 

  • Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microb 74:7694–7708

    Article  CAS  Google Scholar 

  • Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp P, Vacelet J, Webster N, Hentschel U, Taylor MW (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576

    Article  CAS  Google Scholar 

  • Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T, Hentschel U (2011) Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5:61–70. https://doi.org/10.1038/ismej.2010.95

    Article  PubMed  Google Scholar 

  • Simister RL, Deines P, Botté ES, Webster NS, Taylor MW (2011) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14:517–524

    Article  Google Scholar 

  • Steinert G, Busch K, Bayer K, Kodami S, Arbizu PM, Kelly M, Mills S, Erpenbeck D, Dohrmann M, Wörheide G, Hentschel U, Schupp PJ (2020) Compositional and quantitative insights into bacterial and Archaeal communities of south pacific deep-sea sponges (Demospongiae and Hexactinellida). Front Microbiol 11:716. https://doi.org/10.3389/fmicb.2020.00716

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Vesth T, Lagesen K, Acar Ö, Ussery D (2013) CMG-biotools, a free workbench for basic comparative microbial genomics. PLOS ONE 8(4):e60120

    Article  CAS  Google Scholar 

  • Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotech 17:241–249

    Article  CAS  Google Scholar 

  • Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S, Horn M, Wagner M (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12:2070–2082

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was funded by the project Ecología larvaria y dispersión de algunas esponjas destructoras de corales CONACYT-SEP (254806). The first author was awarded a Post-Doctoral Fellowship at the Universidad Nacional Autónoma de México (UNAM) in the Instituto de Ciencias del Mar y Limnologia (ICMyl), Mazatlán Unit and received the fellowship from Dirección General de Asuntos del Personal Académico (DGAPA). The first author thanks SAGI and PIF for the support provided in the project. We thank Dr. Benjamín Yañez for sampling and technical help.

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Authors and Affiliations

  1. Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (Unidad Académica Mazatlán), Mazatlán, México

    Adrián González-Castillo & José Luis Carballo

  2. Laboratorio de Biología Marina, Departamento de Zoología, Universidad de Sevilla, Avda. Reina Mercedes, 6, 41012, Sevilla, Spain

    José Luis Carballo

  3. Laboratorio de Ecología Marina, Centro de Investigaciones Costeras, Centro Universitario de la Costa, Universidad de Guadalajara, Puerto Vallarta, México

    Eric Bautista-Guerrero

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  1. Adrián González-Castillo
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Adrián González-Castillo Data Curation, Writing–Original Draft and Formal analysis. José Luis Carballo Funding acquisition and Conceptualization. Eric Bautista-Guerrero Project administration and Resources.

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Correspondence to Adrián González-Castillo.

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We declare that this manuscript is original and it has not been published before, also it is not currently being considered for publication elsewhere. We also, declare that we have no conflict of interest associated with this publication, and there has not been financial support for this work that could have influenced its outcome. As Corresponding Author, I confirm that the manuscript has been read and approved for submission by all the named authors.

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González-Castillo, A., Carballo, J.L. & Bautista-Guerrero, E. Genomics and phylogeny of the proposed phylum ‘Candidatus Poribacteria’ associated with the excavating sponge Thoosa mismalolli. Antonie van Leeuwenhoek 114, 2163–2174 (2021). https://doi.org/10.1007/s10482-021-01670-z

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