Diversity of a bacterial community associated with Cliona lobata Hancock and Gelliodes pumila (Lendenfeld, 1887) sponges on the South-East coast of India.
Alphaproteobacteria
/ classification
Animals
Arsenic
Bacteria
/ classification
Biodiversity
Cadmium
Climate
Cluster Analysis
High-Throughput Nucleotide Sequencing
India
Lead
Mercury
Metagenome
Metals, Heavy
Microbiota
Phylogeny
Porifera
/ microbiology
Quality Control
RNA, Ribosomal, 16S
/ genetics
Seaweed
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 07 2020
14 07 2020
Historique:
received:
16
11
2019
accepted:
13
05
2020
entrez:
16
7
2020
pubmed:
16
7
2020
medline:
23
1
2021
Statut:
epublish
Résumé
Marine sponges are sources of various bioactive metabolites, including several anticancer drugs, produced mainly by sponge-associated microbes. Palk Bay, on the south-east coast of India, is an understudied, highly disturbed reef environment exposed to various anthropogenic and climatic stresses. In recent years, Palk Bay suffered from pollution due to the dumping of untreated domestic sewage, effluents from coastal aquaculture, tourism, salt pans, cultivation of exotic seaweeds, and geogenic heavy-metal pollution, especially arsenic, mercury, cadmium, and lead. Low microbial-abundant sponge species, such as Gelliodes pumila and Cliona lobata, were found to be ubiquitously present in this reef environment. Triplicate samples of each of these sponge species were subjected to Illumina MiSeq sequencing using V3-V4 region-specific primers. In both C. lobata and G. pumila, there was an overwhelming dominance (98 and 99%) of phylum Candidatus Saccharibacteria and Proteobacteria, respectively. The overall number of operational taxonomic units (OTUs) was 68 (40 and 13 OTUs unique to G. pumila and C. lobata, respectively; 15 shared OTUs). Alphaproteobacteria was the most abundant class in both the sponge species. Unclassified species of phylum Candidatus Saccharibacteria from C. lobata and Chelotivorans composti from G. pumila were the most abundant bacterial species. The predominance of Alphaproteobacteria also revealed the occurrence of various xenobiotic-degrading, surfactant-producing bacterial genera in both the sponge species, indirectly indicating the possible polluted reef status of Palk Bay. Studies on sponge microbiomes at various understudied geographical locations might be helpful in predicting the status of reef environments.
Identifiants
pubmed: 32665602
doi: 10.1038/s41598-020-67717-9
pii: 10.1038/s41598-020-67717-9
pmc: PMC7360593
doi:
Substances chimiques
Metals, Heavy
0
RNA, Ribosomal, 16S
0
Cadmium
00BH33GNGH
Lead
2P299V784P
Mercury
FXS1BY2PGL
Arsenic
N712M78A8G
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11558Références
de Voogd, N. J., Cleary, D. F. R., Polonia, A. R. M. & Gomes, N. C. M. Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, West Java Indonesia. FEMS Microbiol. Ecol. 91, fiv019 (2015).
pubmed: 25764467
Pita, L., Rix, L., Slaby, B. M., Franke, A. & Hentschel, U. The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6, 46 (2018).
pubmed: 29523192
pmcid: 5845141
Yang, Q., Franco, C. M. M. & Zhang, W. Uncovering the hidden marine sponge microbiome by applying a multi-primer approach. Sci. Rep. 9, 6214 (2019).
pubmed: 30996336
pmcid: 6470215
Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Ann. Rev. Microbiol. 70, 317–340 (2016).
Vargas, S. et al. Barcoding sponges: an overview based on comprehensive sampling. PLoS ONE 7, e39345–e39345 (2012).
pubmed: 22802937
pmcid: 3389008
Van Soest, R. W. M. et al. Global diversity of sponges (Porifera). PLoS ONE 7, e35105 (2012).
pubmed: 22558119
pmcid: 3338747
Hentschel, U. & Hopke, J. Molecular evidence for a uniform microbial community in sponges from different oceans. FEMS Microb. Ecol. 55, 167–177 (2002).
Lee, Y. K., Lee, J. H. & Lee, H. K. Microbial symbiosis in marine sponges. J. Microbiol. 39, 254–264 (2000).
Maldonado, M. et al. Aggregated clumps of lithistid sponges: a singular, reef-like bathyal habitat with relevant paleontological connections. PLoS ONE 10, e0125378 (2015).
pubmed: 26016786
pmcid: 4446211
Cleary, D. F. R., Polónia, A. R. M. & de Voogd, N. J. Bacterial Communities Inhabiting the Sponge Biemna fortis, Sediment and Water in Marine Lakes and the Open Sea. Microb. Ecol. 76, 610–624 (2018).
pubmed: 29470608
Bell, J. J., Davy, S. K., Jones, T., Taylor, M. W. & Webster, N. S. Could some coral reefs become sponge reefs as our climate changes?. Glob. Chang. Biol. 19, 2613–2624 (2013).
pubmed: 23553821
Wulff, J. Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biol. Conserv. Biol Conserv 127, 167–176 (2006).
O’Brien, P. A., Morrow, K. M., Willis, B. L. & Bourne, D. G. Implications of ocean acidification for marine microorganisms from the free-living to the host-associated. Front. Mar. Sci. 3, 47 (2016).
McDevitt-Irwin, J. M., Baum, J. K., Garren, M. & Vega Thurber, R. L. Responses of coral-associated bacterial communities to local and global stressors. Front. Mar. Sci. 4, 262 (2017).
Kiran, G. S. et al. Production of lipopeptide biosurfactant by a marine Nesterenkonia sp. and its application in food industry. Front. Microbiol. 8, 1138 (2017).
pubmed: 28702002
pmcid: 5488535
Konstantinou, D., Gerovasileiou, V., Voultsiadou, E. & Gkelis, S. Sponges-cyanobacteria associations: global diversity overview and new data from the eastern Mediterranean. PLoS ONE 13, e0195001–e0195001 (2018).
pubmed: 29596453
pmcid: 5875796
Gilbert, J. A., Jansson, J. K. & Knight, R. The earth microbiome project: successes and aspirations. BMC Biol. 12, 69 (2014).
pubmed: 25184604
pmcid: 4141107
Moitinho-Silva, L. et al. The sponge microbiome project. Gigascience 6, 1–7 (2017).
pubmed: 29020741
Thinesh, T., Arul Jose, P., Hassan, S., Muthamizh Selvan, K. & Selvin, J. Intrusion of coral-killing sponge (Terpios hoshinota) on the reef of Palk Bay. Curr. Sci. 109, 1030–1032 (2015).
Thinesh, T., Meenatchi, R., Jose, P. A., Kiran, G. S. & Selvin, J. Differential bleaching and recovery pattern of southeast Indian coral reef to 2016 global mass bleaching event: occurrence of stress-tolerant symbiont Durusdinium (Clade D) in corals of Palk Bay. Mar. Pollut. Bull. 145, 287–294 (2019).
pubmed: 31590790
Easson, C. G. & Thacker, R. W. Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front. Microbiol. 5, 532 (2014).
pubmed: 25368606
pmcid: 4201110
Thinesh, T., Mathews, G. & Edward, J. K. P. Outbreaks of Acropora white syndrome and Terpios sponge overgrowth combined with coral mortality in Palk Bay, southeast coast of India. Dis. Aquat. Organ. 126, 63–70 (2017).
pubmed: 28930086
Taylor, M. W., Radax, R., Steger, D. & Wagner, M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71, 295–347 (2007).
pubmed: 17554047
pmcid: 1899876
Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 10, 641–654 (2012).
pubmed: 22842661
Schmitt, S. et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6, 564–576 (2012).
pubmed: 21993395
Abdelmohsen, U. R., Bayer, K. & Hentschel, U. Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat. Prod. Rep. 31, 381–399 (2014).
pubmed: 24496105
Fieseler, L., Horn, M., Wagner, M. & Hentschel, U. Discovery of the novel candidate phylum ‘Poribacteria’ in marine sponges. Appl. Environ. Microbiol. 70, 3724–3732 (2004).
pubmed: 15184179
pmcid: 427773
Souza, D. T. et al. Analysis of bacterial composition in marine sponges reveals the influence of host phylogeny and environment. FEMS Microbiol. Ecol. 93, 1 (2016).
Simister, R., Taylor, M. W., Tsai, P. & Webster, N. Sponge-microbe associations survive high nutrients and temperatures. PLoS ONE 7, e52220–e52220 (2012).
pubmed: 23284943
pmcid: 3527390
Thrash, J. C. et al. Metabolic roles of uncultivated bacterioplankton lineages in the Northern Gulf of Mexico “Dead Zone”. MBio 8, e01017-e1117 (2017).
pubmed: 28900024
pmcid: 5596340
Lücker, S. et al. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc. Natl. Acad. Sci. 107, 13484 (2010).
Bundy, C. A. et al. Enhanced denitrification in Downflow Hanging Sponge reactors for decentralised domestic wastewater treatment. Bioresour. Technol. 226, 1–8 (2017).
pubmed: 27951508
Ahn, C. H., Park, H. D., Lee, Y. O. & Park, J. K. Appearance of novel G-bacteria belonging to acidobacteria in a dairy wastewater treatment plant. Environ. Technol. 29, 497–504 (2008).
pubmed: 18661733
Silva-Bedoya, L. M., Sánchez-Pinzón, M. S., Cadavid-Restrepo, G. E. & Moreno-Herrera, C. X. Bacterial community analysis of an industrial wastewater treatment plant in Colombia with screening for lipid-degrading microorganisms. Microbiol. Res. 192, 313–325 (2016).
pubmed: 27664750
Cydzik-Kwiatkowska, A. & Zielińska, M. Bacterial communities in full-scale wastewater treatment systems. World J. Microbiol. Biotechnol. 32, 66 (2016).
pubmed: 26931606
pmcid: 4773473
Collingro, A. et al. Recovery of an environmental Chlamydia strain from activated sludge by co-cultivation with Acanthamoeba sp.. Microbiol. 151, 301–309 (2005).
Ouyang, E., Liu, Y., Ouyang, J. & Wang, X. Effects of different wastewater characteristics and treatment techniques on the bacterial community structure in three pharmaceutical wastewater treatment systems. Environ. Technol. 40, 329–341 (2019).
pubmed: 29037124
Sood A., Renuka N., Prasanna R., & Ahluwalia A.S. Cyanobacteria as potential options for wastewater treatment. (eds. Ansari A., Gill S., Gill R., Lanza G., & Newman L.), Phytoremediation, pp. 83–93 (Springer, 2015).
Palanichamy, S. & Rajendran, A. Heavy metal concentration in seawater and sediment of Gulf of Mannar and Palk Bay, southeast coast of India. Ind. J. Mar. Sci. 29, 116–119 (2000).
Baby, L. et al. Comparison of hydrographic and sediment characteristics of seagrass meadows of Gulf of Mannar and Palk Bay, South West Coast of India. Int. J. Fis. Aqu. Stud. 5, 80–84 (2017).
Rajkumar, M., Aravind, R. & Pandey, A. K. Flora and fauna of coral reef habitats excluding fishes. Econ. Environ. Cons. 19, 1073–1078 (2013).
Pillai, C. S. G. Composition of the coral fauna of the southeastern coast of India and the Laccadives. in Regional variation in Indian Ocean coral reefs (eds Stoddart, D. R. & Young, C. M.) Symp. Zool. Soc. Lond., 28, 301–327 (1971).
Meera, B. Prevalence of pollution indicators in palkbay coastal zone, southern India. Int. J. Adv. Sci. Res. 2, 027–031 (2016).
Dawson, M. N., Raskoff, K. A. & Jacobs, D. K. Field preservation of marine invertebrate tissue for DNA analysis. Mol. Mar. Microbiol. 7, 145–152 (1998).
Sivaleela, G. S. Marine sponges of Gulf of Mannar and Palk Bay. Rec. Zool. Surv. India 114, 607–622 (2014).
von Lendenfeld, R. Die Chalineen des australischen Gebietes Zoologische Jahrbücher. Jena. 2, 723–828 (1887).
Hancock, A. On the excavating powers of certain sponges belonging to the genus Cliona with descriptions of several new Species, and an allied generic form. Ann. Mag. Nat. His. 3, 321–348 (1849).
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
pubmed: 23955772
Kindt, R., & Kindt, M. R. Package Biodiversity R (2019).
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Wickham H. ggplot2: elegant graphics for data analysis. Springer, New York. ISBN 978-3-319-24277-4 (2016). https://ggplot2.tidyverse.org .
Hammer, Ø, Harper, D. A. T. & Ryan, P. D. Past: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).
Oliveira, C. et al. 16S rRNA gene-based metagenomic analysis of Ozark cave bacteria. Diversity 9, 31 (2017).
pubmed: 29551950
pmcid: 5856467
Kanehisa, M., Goto, S., Sato, Y., Furumichi, M. & Tanabe, M. KEGG for integration and interpretation of large-scale molecular data sets. Nucl. Acids Res. 40, D109–D114 (2012).
pubmed: 22080510