Exploring the microbial community and biotechnological potential of the sponge Xestospongia sp. from an anchialine cave in the Yucatán Peninsula

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Pablo Suárez-Moo
Ninette C García-Martínez
Norma A Márquez-Velázquez
Mario Figueroa
Eric Allen
Alejandra Prieto-Davó


Sponge-associated microorganisms are key influencers of nutrient biogeochemistry and important sources of bioactive natural products. This study provides the first insights into the taxonomic diversity of the microbial community associated with the sponge Xestospongia sp. from an anchialine cave in the coastal area of the underground river of the Yucatán Peninsula in Xcalak, Quintana Roo, Mexico, and the potential antimicrobial activity of its cultivable bacteria. High abundances of Sulfurospirillum and Desulfovibrio were detected with 16S rRNA amplicons, suggesting that the microbial community of Xestospongia sp. plays an important role in the geochemical sulfur cycle. Analysis with crude extracts of Nocardiopsis dasonvillei NCA-454 revealed antimicrobial activity against methicillin-sensitive Staphylococcus aureus ATCC 25913 (MSSA) and methicillin-​resistant ​S. aureus ATCC 43300 (MRSA). Studies of the microbiomes of sponges from the anchialine cave system in the Yucatán Peninsula can help elucidate the biogeochemical cycles of these poorly studied environments. Moreover, the microorganisms of these microbial communities represent an untapped source of secondary metabolites with biotechnological potential.


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Suárez-Moo, P., García-Martínez, N. C., Márquez-Velázquez, N. A., Figueroa, M., Allen, E., & Prieto-Davó, A. (2024). Exploring the microbial community and biotechnological potential of the sponge Xestospongia sp. from an anchialine cave in the Yucatán Peninsula. Ciencias Marinas, 50. https://doi.org/10.7773/cm.y2024.3442
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Almeida JF, Marques M, Oliveira V, Egas C, Mil-Homens D, Viana R, Cleary DFR, Huang YM, Fialho AM, Teixeira MC, et al. 2023. Marine sponge and octocoral-associated bacteria show versatile secondary metabolite biosynthesis potential and antimicrobial activities against human pathogens. Mar Drugs. 21(1):34. https://doi.org/10.3390/md21010034 DOI: https://doi.org/10.3390/md21010034

Bauer-Gottwein P, Gondwe BRN, Charvet G, Marín LE, Rebolledo-Vieyra M, Merediz-Alonso G. 2011. Review: The Yucatán Peninsula karst aquifer, Mexico. Hydrogeol J. 19(3):507-524. https://doi.org/10.1007/s10040-010-0699-5 DOI: https://doi.org/10.1007/s10040-010-0699-5

Bennur T, Ravi Kumar A, Zinjarde SS, Javdekar V. 2016. Nocardiopsis species: A potential source of bioactive compounds. J Appl Microbiol. 120(1):1-16. https://doi.org/10.1111/jam.12950 DOI: https://doi.org/10.1111/jam.12950

Bhairamkar S, Kadam P, Anjulal H, Joshi A, Chaudhari R, Bagul D, Javdekar V, Zinjarde S. 2023. Comprehensive updates on the biological features and metabolic potential of the versatile extremophilic actinomycete Nocardiopsis dassonvillei. Res Microbiol. 21(4):104171. https://doi.org/10.1016/j.resmic.2023.104171 DOI: https://doi.org/10.1016/j.resmic.2023.104171

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, AlGhalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 37:852-857. https://doi.org/10.1038/s41587-019-0209-9 DOI: https://doi.org/10.1038/s41587-019-0209-9

Brinkmann CM, Marker A, Kurtböke Dİ. 2017. An overview on marine sponge-symbiotic bacteria as unexhausted sources for natural product discovery. Diversity. 9(4):40. https://doi.org/10.3390/d9040040 DOI: https://doi.org/10.3390/d9040040

Busch K, Slaby BM, Bach W, Boetius A, Clefsen I, Colaço A, Creemers M, Cristobo J, Federwisch L, Franke A, et al. 2022. Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome. Nat Commun. 13:5160. https://doi.org/10.1038/s41467-022-32684-4 DOI: https://doi.org/10.1038/s41467-022-33966-7

Calderón-Gutiérrez F, Solís-Marín FA, Gómez P, Sánchez C, Hernández-Alcántara P, Álvarez-Noguera F, Yáñez-Mendoza G. 2017. Mexican anchialine fauna — With emphasis in the high biodiversity cave El Aerolito. Reg Stud Mar Sci. 9:43-55. https://doi.org/10.1016/j.rsma.2016.11.001 DOI: https://doi.org/10.1016/j.rsma.2016.11.001

Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6(8):1621-1624. https://doi.org/10.1038/ismej.2012.8 DOI: https://doi.org/10.1038/ismej.2012.8

Deshpande A, Thakur N. 2020. Chemical ecology driven bioprospecting of marine sponges. In: Kim S (ed.), Encyclopedia of Marine Biotechnology. 1st ed: Wiley. p. 681-692. https://doi.org/10.1002/9781119143802.ch25 DOI: https://doi.org/10.1002/9781119143802.ch25

Elfeky HH, Hanora A, Solyman SM. 2023. Bioactivity of bacteria associated with Red Sea nudibranchs and whole genome sequence of Nocardiopsis dassonvillei RACA-4. Mar Genomics. 67:101004. https://doi.org/10.1016/j.margen.2022.101004 DOI: https://doi.org/10.1016/j.margen.2022.101004

Fauque GD. 1994. Sulfur reductase from thiophilic sulfate-reducing bacteria. Methods Enzymol. 243:353-367. https://doi.org/10.1016/0076-6879(94)43026-8 DOI: https://doi.org/10.1016/0076-6879(94)43026-8

Feng G, Sun W, Zhang F, Karthik L, Li Z. 2016. Inhabitancy of active Nitrosopumilus-like ammonia-oxidizing archaea and Nitrospira nitrite-oxidizing bacteria in the sponge Theonella swinhoei. Sci Rep. 26(6):24966. https://doi.org/10.1038/srep24966 DOI: https://doi.org/10.1038/srep24966

Foster ZSL, Sharpton TJ, Grunwald NJ. 2017. Metacoder: An R package for visualization and manipulation of community taxonomic diversity data. PLoS Comput Biol. 13(2):e1005404. https://doi.org/10.1371/journal.pcbi.1005404 DOI: https://doi.org/10.1371/journal.pcbi.1005404

Freeman CJ, Easson CG, Matterson KO, Thacker RW, Baker DM, Paul VJ. 2020. Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association. The ISME J. 14(6):1571-1583. https://doi.org/10.1038/s41396-020-0625-3 DOI: https://doi.org/10.1038/s41396-020-0625-3

Gerovasileiou V, Voultsiadou E. 2012. Marine caves of the Mediterranean Sea: A sponge biodiversity reservoir within a biodiversity hotspot. PLoS ONE. 7(7):1-17. https://doi.org/10.1371/journal.pone.0039873 DOI: https://doi.org/10.1371/journal.pone.0039873

Gómez P, Calderón-Gutiérrez F. 2020. Anchialine cave-dwelling sponge fauna (Porifera) from La Quebrada, Mexico, with the description of the first Mexican stygobiont sponges. Zootaxa. 4803(1):125-151. https://doi.org/10.11646/zootaxa.4803.1.7 DOI: https://doi.org/10.11646/zootaxa.4803.1.7

Goris T, Gabriele D. 2016. The Genus Sulfurospirillum. In: Adrian L, Löffler FE (eds.), Organohalide-Respiring Bacteria. Berlin (Germany): Springer. p. 1-632. https://doi.org/10.1007/978-3-662-49875-0 DOI: https://doi.org/10.1007/978-3-662-49875-0_10

Haber M, Burgsdorf I, Handley KM, Rubin-Blum M, Steindler L. 2021. Genomic insights into the lifestyles of Thaumarchaeota inside sponges. Front Microbiol. 11:622824. https://doi.org/10.3389/fmicb.2020.622824 DOI: https://doi.org/10.3389/fmicb.2020.622824

Hayami Y, Ambalavanan L, Zainathan SC, Danish-Daniel M, Sharifah NE, Iehata S. 2023. Diversity and functional roles of the symbiotic microbiome associated to marine sponges off Karah Island, Terengganu, Malaysia. Reg Stud Mar Sci. 62. https://doi.org/10.1016/j.rsma.2023.102967 DOI: https://doi.org/10.1016/j.rsma.2023.102967

Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M. 2003. Microbial Diversity of Marine Sponges. In: Müller WEG (ed.), Sponges (Porifera). Volume 37: Springer. p. 59-88.https://doi.org/10.1007/978-3-642-55519-0_3 DOI: https://doi.org/10.1007/978-3-642-55519-0_3

Hoffmann F, Larsen O, Thiel V, Rapp HT, Pape T, Michaelis W, Reitner J. 2005. An anaerobic world in sponges. Geomicrobiol J. 22(1–2):1-10. https://doi.org/10.1080/01490450590922505 DOI: https://doi.org/10.1080/01490450590922505

Indraningrat AAG, Steinert G, Becking LE, Mueller B, de Goeij JM, Smidt H, Sipkema D. 2022. Sponge holobionts shift their prokaryotic communities and antimicrobial activity from shallow to lower mesophotic depths. Antonie van Leeuwenhoek. 115:1265-1283. https://doi.org/10.1007/s10482-022-01770-4 DOI: https://doi.org/10.1007/s10482-022-01770-4

Jahn M, Vialas V, Karlsen J, Maddalo G, Edfors F, Forsström B, Uhlén M, Käll L, Hudson EP. 2018. Growth of Cyanobacteria is constrained by the abundance of light and carbon assimilation proteins. Cell Rep. 25(2):478-486. https://doi.org/10.1016/j.celrep.2018.09.040 DOI: https://doi.org/10.1016/j.celrep.2018.09.040

Jayatilake GS, Thornton MP, Leonard AC, Grimwade JE, Baker BJ. 1996. Metabolites from an Antarctic sponge-associated bacterium, Pseudomonas aeruginosa. J Nat Prod. 59(3):293-296. https://doi.org/10.1021/np960095b DOI: https://doi.org/10.1021/np960095b

Kennedy J, Flemer B, Jackson SA, Morrissey JP, O’Gara F, Dobson ADW. 2014. Evidence of a putative deep sea specific microbiome in marine sponges. PLoS ONE. 9(3):e91092. https://doi.org/10.1371/journal.pone.0091092 DOI: https://doi.org/10.1371/journal.pone.0091092

Komaki H, Ichikawa N, Hosoyama A, Fujita N, Igarashi Y. 2014. Draft genome sequence of marine-derived Actinomycete Nocardiopsis sp. strain TP-A0876, a producer of polyketide pyrones. Genome Announc. 2(4):e00665-14. https://doi.org/10.1128/genomea.00665-14 DOI: https://doi.org/10.1128/genomeA.00665-14

Law KP, He W, Tao J, Zhang C. 2021. Characterization of the exometabolome of Nitrosopumilus maritimus SCM1 by liquid chromatography-ion mobility mass spectrometry. Front Microbiol. 12:658781. https://doi.org/10.3389/fmicb.2021.658781 DOI: https://doi.org/10.3389/fmicb.2021.658781

Leal CV, Avelino-Alves D, Salazar V, Omachi C, Thompson C, Berlinck RGS, Hajdu E, Thompson F. 2022. Sponges present a core prokaryotic community stable across Tropical Western Atlantic. Sci Total Environ. 835:155145. https://doi.org/10.1016/j.scitotenv.2022.155145. DOI: https://doi.org/10.1016/j.scitotenv.2022.155145

Lesser MP, Fiore C, Slattery M, Zaneveld J. 2016. Climate change stressors destabilize the microbiome of the Caribbean barrel sponge, Xestospongia muta. J Exp Mar Bio Ecol. 475:11-18. https://doi.org/10.1016/j.jembe.2015.11.004. DOI: https://doi.org/10.1016/j.jembe.2015.11.004

Lesser MP, Pankey MS, Slattery M, Macartney KJ, Gochfeld DJ. 2022. Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges. ISME Commun. 2(1):1-12. https://doi.org/10.1038/s43705-022-00196-3 DOI: https://doi.org/10.1038/s43705-022-00196-3

Li P, Lu H, Zhang Y, Zhang X, Liu L, Wang M, Liu L. 2023. The natural products discovered in marine sponge-associated microorganisms: structures, activities, and mining strategy. Front mar sci. 10. https://doi.org/10.3389/fmars.2023.1191858 DOI: https://doi.org/10.3389/fmars.2023.1191858

Moitinho-Silva L, Nielsen S, Amir A, Gonzalez A, Ackermann GL, Cerrano C, Astudillo-Garcia C, Easson C, Sipkema D, Liu F, et al. 2017. The sponge microbiome project. GigaScience. 6(10):1-13. https://doi.org/10.1093/gigascience/gix077 DOI: https://doi.org/10.1093/gigascience/gix077

Nakagawa T, Koji M, Hosoyama A, Yamazoe Yuki A, Tsuchiya Y, Ueda S, Takahashi R, Stahl DA. 2021. Nitrosopumilus zosterae sp. nov, an autotrophic ammonia-oxidizing archaeon of phylum Thaumarchaeota isolated from coastal eelgrass sediments of Japan. IJSEM. 71(8):004961. https://doi.org/10.1099/ijsem.0.004961 DOI: https://doi.org/10.1099/ijsem.0.004961

Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. 2017. MetaSPAdes: a new versatile metagenomic assembler. Genome Res. 27:824-834. https://doi.org/10.1101/gr.213959.116 DOI: https://doi.org/10.1101/gr.213959.116

Perry E, Paytan A, Pedersen B, Velazquez-Oliman G. 2009. Groundwater geochemistry of the Yucatán Peninsula, Mexico: Constraints on stratigraphy and hydrogeology. J Hydrol. 367(1–2):27-40. https://doi.org/10.1016/j.jhydrol.2008.12.026 DOI: https://doi.org/10.1016/j.jhydrol.2008.12.026

R Studio Team. 2015. RStudio: Integrated Development for R. Boston (MA): R Studio PBC. http://www.rstudio.com/.

Radjasa OK, Vaske YM, Navarro G, Vervoort HC, Tenney K, Linington RG, Crews P. 2011. Highlights of marine invertebrate-derived biosynthetic products: Their biomedical potential and possible production by microbial associants. Bioorg Med Chem. 19(22):6658-6674. https://doi.org/10.1016/j.bmc.2011.07.017 DOI: https://doi.org/10.1016/j.bmc.2011.07.017

Santos OCS, Soares AR, Machado FLS, Romanos MTV, Muricy G, Giambiagi-deMarval M, Laport MS. 2015. Investigation of biotechnological potential of sponge-associated bacteria collected in Brazilian coast. Lett Appl Microbiol. 60(2):140-147. https://doi.org/10.1111/lam.12347 DOI: https://doi.org/10.1111/lam.12347

Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, et al. 2012. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6(3):564-576. https://doi.org/10.1038/ismej.2011.116 DOI: https://doi.org/10.1038/ismej.2011.116

Schmitter-Soto JJ, Comín FA, Escobar-Briones E, Herrera-Silveira J, Alcocer J, Suárez-Morales E, Elías-Gutiérrez M, Díaz-Arce V, Marín LE, Steinich B. 2002. Hydrogeochemical and biological characteristics of cenotes in the Yucatán Peninsula (SE Mexico). Hydrobiologia. 467:215-228. https://doi.org/10.1023/A:1014923217206 DOI: https://doi.org/10.1007/978-94-010-0415-2_19

Selvin J, Shanmughapriya S, Gandhimathi R, Seghal Kiran G, Rajeetha Ravji T, Natarajaseenivasan K, Hema TA. 2009. Optimization and production of novel antimicrobial agents from sponge associated marine actinomycetes Nocardiopsis dassonvillei MAD08. Appl Microbiol Biotechnol. 83(3):435-445. https://doi.org/10.1007/s00253-009-1878-y DOI: https://doi.org/10.1007/s00253-009-1878-y

Su P, Wang DX, Ding SX, Zhao J. 2014. Isolation and diversity of natural product biosynthetic genes of cultivable bacteria associated with marine sponge Mycale sp. from the coast of Fujian, China. Can J Microbiol. 60(4):217-25. https://doi.org/10.1139/cjm-2013-0785 DOI: https://doi.org/10.1139/cjm-2013-0785

Suárez-Moo P, Haro-Moreno JM, Rodriguez-Valera F. 2024. Microdiversity in marine pelagic ammonia-oxidizing archaeal populations. bioRxiv:590705. https://doi.org/10.1101/2024.04.23.590705 DOI: https://doi.org/10.1101/2024.04.23.590705

Suárez-Moo P, Remes-Rodríguez CA, Márquez-Velázquez NA, Falcón LI, García-Maldonado JQ, Prieto-Davó A. 2022. Changes in the sediment microbial community structure of coastal and inland sinkholes of a karst ecosystem from the Yucatán peninsula. Sci Rep. 12(1):1-11. https://doi.org/10.1038/s41598-022-05135-9 DOI: https://doi.org/10.1038/s41598-022-05135-9

Thakur NL, Perović-Ottstadt S, Batel R, Korzhev M, Diehl-Seifert B, Müller IM, Müller WEG. 2005. Innate immune defense of the sponge Suberites domuncula against gram-positive bacteria: Induction of lysozyme and AdaPTin. Mar Biol. 146(2):271-282. https://doi.org/10.1007/s00227-004-1438-z DOI: https://doi.org/10.1007/s00227-004-1438-z

Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, Olson JB, Erwin PM, López-Legentil S, Luter H, et al. 2016. Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun. 7:11870. https://doi.org/10.1038/ncomms11870 DOI: https://doi.org/10.1038/ncomms11870

Tian RM, Sun J, Cai L, Zhang WP, Zhou GW, Qiu JW, Qian PY. 2016. The deep-sea glass sponge Lophophysema eversa harbours potential symbionts responsible for the nutrient conversions of carbon, nitrogen and sulfur. Environ Microbiol. 18(8):2481-2494. https://doi.org/10.1111/1462-2920.13161 DOI: https://doi.org/10.1111/1462-2920.13161

Weisburg W, Barns S, Pelletier D, Lane D. 1991. 16S ribosomal DNA amplification for phylogenetic study. J Bacterial. 173:697-703. https://doi.org/10.1128/jb.173.2.697-703.1991 DOI: https://doi.org/10.1128/jb.173.2.697-703.1991

Yang Q, Franco CMM, Zhang W. 2019. Uncovering the hidden marine sponge microbiome by applying a multi-primer approach. Sci Rep. 9(1):1-13. https://doi.org/10.1038/s41598-019-42694-w DOI: https://doi.org/10.1038/s41598-019-42694-w

Zhang D, Sun W, Feng G, Zhang F, Anbuchezhian R, Li Z, Jiang Q. 2015. Phylogenetic diversity of sulphate-reducing Desulfovibrio associated with three South China Sea sponges. Lett Appl Microbiol. 60(5):504-512. https://doi.org/10.1111/lam.12400 DOI: https://doi.org/10.1111/lam.12400

Zheng Y, Wang B, Gao P, Yang Y, Xu B, Su X, Ning D, Tao Q, Li Q, Zhao F, et al. 2024. Novel order-level lineage of ammonia-oxidizing archaea. ISME J. 18:1-13. https://doi.org/10.1093/ismejo/wrad002 DOI: https://doi.org/10.1093/ismejo/wrad002