Skip to main content
SpringerLink
Log in

Enteromorpha prolifera Diet Drives Intestinal Microbiome Composition in Siganus oramin

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Enteromorpha prolifera (E. prolifera) contains complex sulfated polysaccharides that are resistant to biological degradation. Most organisms cannot digest biomass of E. prolifera, except Siganus oramin (S. oramin). This study was conducted to identify the bacteria in the intestine of S. oramin facilitating the digestion of E. prolifera polysaccharides (EPP). Metagenomic sequencing analysis of the S. oramin intestinal microbiota revealed that E. prolifera diet increased the number of Firmicutes, replacing Proteobacteria to be the dominant bacteria. The proportion of Firmicutes increased from 38.8 to 58.6%, with Bacteroidetes increasing nearly fivefold from 5 to 23.7%. 16S rDNA high-throughput sequencing showed that EPP-induced Bacteroidetes increased significantly in the intestinal flora of S. oramin cultivated in vitro. Metatranscriptome analysis showed that EPP induced more transferase, polysaccharide hydrolase, glycoside hydrolase, and esterases expressed in vitro, and most of them were taxonomically annotated to Bacteroidetes. Compared with the aggregation of GH family genes in metagenomic sequencing analysis in vivo, EPP induced more CBM32, GH2, GT2, GT30, and GH30 families gene expression in vitro. In general, We found that the bacteria in intestinal tract of S. oramin responsible for digestion of E. prolifera were Firmicutes and Bacteroidetes, while Bacteroidetes was the dominant bacteria involved in EPP degradation in vitro cultures. Compared with in vivo experiments, only GH family genes were mostly involved, we detected a more complete and complex EPP degradation pathway in vitro. The results may benefit the further study of biodegradation of E. prolifera and has potential implications for the utilization of E. prolifera for biotechnology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

All raw sequence data have been submitted to GenBank under the Accession Numbers PRJNA597698, PRJNA597688, and PRJNA598103.

References

  1. Li H, Zhang Y, Chen J et al (2019) Nitrogen uptake and assimilation preferences of the main green tide alga Ulva prolifera in the Yellow Sea, China. J Appl Phycol 31:625–635. https://doi.org/10.1007/s10811-018-1575-2

    Article  CAS  Google Scholar 

  2. Vivtor S, Adriana Z (2013) Green and golden seaweed tides on the rise. Nature 504:84–88. https://doi.org/10.1038/nature12860

    Article  CAS  Google Scholar 

  3. Ficko-Blean E, Cecile H, Gurvan M (2015) Sweet and sour sugars from the sea: the biosynthesis and remodeling of sulfated cell wall polysaccharides from marine macroalgae. Perspect Phycol 2(1):51–64. https://doi.org/10.1127/pip/2015/0028

    Article  Google Scholar 

  4. Popper ZA, Michel G, Hervé C et al (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62(1):567–590. https://doi.org/10.1146/annurev-arplant-042110-103809

    Article  CAS  PubMed  Google Scholar 

  5. Li D, Chen L, Zhao J et al (2010) Evaluation of the pyrolytic and kinetic characteristics of Enteromorpha prolifera as a source of renewable biofuel from the Yellow Sea of China. Chem Eng Res Des 88(5–6):647–652. https://doi.org/10.1016/j.cherd.2009.10.011

    Article  CAS  Google Scholar 

  6. Zhao C, Ruan L (2011) Biodegradation of Enteromorpha prolifera by mangrove degrading micro-community with physical–chemical pretreatment. Appl Microbiol Biotechnol 92(4):709–716. https://doi.org/10.1007/s00253-011-3384-2

    Article  CAS  PubMed  Google Scholar 

  7. Shi M, Wei X, Xu J et al (2017) Carboxymethylated degraded polysaccharides from Enteromorpha prolifera: preparation and in vitro antioxidant activity. Food Chem 215:76–83. https://doi.org/10.1016/j.foodchem.2016.07.151

    Article  CAS  PubMed  Google Scholar 

  8. Yuan X, Zheng J, Ren L et al (2019) Enteromorpha prolifera oligomers relieve pancreatic injury in streptozotocin (STZ)-induced diabetic mice. Carbohydr Polym 206:403–411. https://doi.org/10.1016/j.carbpol.2018.11.019

    Article  CAS  PubMed  Google Scholar 

  9. Ye H, Shen Z, Cui J et al (2019) Hypoglycemic activity and mechanism of the sulfated rhamnose polysaccharides chromium (III) complex in type 2 diabetic mice. Bioorg Chem 88:1029–1042. https://doi.org/10.1016/j.bioorg.2019.102942

    Article  CAS  Google Scholar 

  10. Liu X, Liu D, Lin G et al (2019) Anti-ageing and antioxidant effects of sulfate oligosaccharides from green algae Ulva lactuca and Enteromorpha prolifera in SAMP8 mice. Int J Biol Macromol 139:342–351. https://doi.org/10.1016/j.ijbiomac.2019.07.195

    Article  CAS  PubMed  Google Scholar 

  11. Shanmugam S, Ngo H-H, Yi-Rui Wu (2020) Advanced CRISPR/Cas-based genome editing tools for microbial biofuels production: a review. Renew Energy 149:1107–1119. https://doi.org/10.1016/j.renene.2019.10.107

    Article  CAS  Google Scholar 

  12. Pitlik SD, Koren O (2017) How holobionts get sick-toward a unifying scheme of disease. Microbiome 5(1):64–68. https://doi.org/10.1186/s40168-017-0281-7

    Article  PubMed  PubMed Central  Google Scholar 

  13. Flint HJ, Bayer EA, Rincon MT et al (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6(2):121–131. https://doi.org/10.1038/nrmicro1817

    Article  CAS  PubMed  Google Scholar 

  14. Hehemann JH, Boraston AB, Czjzek M (2014) A sweet new wave: structures and mechanisms of enzymes that digest polysaccharides from marine algae. Curr Opin Struct Biol 28:77–86. https://doi.org/10.1016/j.sbi.2014.07.009

    Article  CAS  PubMed  Google Scholar 

  15. Martin M, Portetelle D, Michel G et al (2014) Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol 98(7):2917–2935. https://doi.org/10.1007/s00253-014-5557-2

    Article  CAS  PubMed  Google Scholar 

  16. Liu W-C, Zhou S-H, Balasubramanian B et al (2020) Dietary seaweed (Enteromorpha) polysaccharides improves growth performance involved in regulation of immune responses, intestinal morphology and microbial community in banana shrimp Fenneropenaeus merguiensis. Fish Shellfish Immunol 104:202–212. https://doi.org/10.1016/j.fsi.2020.05.079

    Article  CAS  PubMed  Google Scholar 

  17. Marjolaine M, Tristan B, Renee M et al (2015) The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria. Front Microbiol 6:1487. https://doi.org/10.3389/fmicb.2015.01487

    Article  Google Scholar 

  18. Gobet A, Mest L, Perennou M et al (2018) Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore. Microbiome 6(1):60–68. https://doi.org/10.1186/s40168-018-0430-7

    Article  PubMed  PubMed Central  Google Scholar 

  19. Dudek M, Adams J, Swain M et al (2014) Metaphylogenomic and potential functionality of the limpet Patella pellucida’s gastrointestinal tract microbiome. Int J Mol Sci 15(10):18819–18839. https://doi.org/10.3390/ijms151018819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhou Y, Wei F, Zhang W et al (2018) Copper bioaccumulation and biokinetic modeling in marine herbivorous fish, Siganus oramin. Aquat Toxicol 196:61–69. https://doi.org/10.1016/j.aquatox.2018.01.009

    Article  CAS  PubMed  Google Scholar 

  21. Zhang Z, Han X, Xu Y et al (2016) Biodegradation of Enteromorpha polysaccharides by intestinal micro-community from Siganus oramin. J Ocean Univ China 15(6):1034–1038. https://doi.org/10.1007/s11802-016-3002-0

    Article  CAS  Google Scholar 

  22. Jiao L, Jiang P, Zhang L et al (2010) Antitumor and immunomodulating activity of polysaccharides from Enteromorpha intestinalis. Biotechnol Bioprocess Eng 15(3):421–428. https://doi.org/10.1007/s12257-008-0269-z

    Article  CAS  Google Scholar 

  23. Han X, Lin B, Ru G et al (2014) Gene cloning and characterization of an α-amylase from Alteromonas macleodii B7 for Enteromorpha polysaccharide degradation. J Microbiol Biotechnol 24(2):254–263. https://doi.org/10.4014/jmb.1304.04036

    Article  CAS  PubMed  Google Scholar 

  24. Watanabe K (1998) Molecular detection, isolation, and physiological characterization of functionally dominant phenol-degrading bacteria in activated sludge. Appl Environ Microbiol 64(11):4396–4402. https://doi.org/10.1080/09583150802488808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Don RH, Cox PT, Wainwright BJ et al (1991) ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19(14):4008. https://doi.org/10.1093/nar/19.14.4008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Urakawa H, Martens-Habbena W, Stahl DA (2010) High abundance of ammonia-oxidizing Archaea in coastal waters, determined using a modified DNA extraction method. Appl Environ Microbiol 76(7):2129–2135. https://doi.org/10.1128/aem.02692-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mettel C, Liesack W (2010) Extraction of mRNA from soil. Appl Environ Microbiol 76(17):5995–6000. https://doi.org/10.1128/AEM.03047-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Terrapon N, Lombard V, Gilbert HJ et al (2015) Automatic prediction of polysaccharide utilization loci in Bacteroidetes species from the human gut microbiota. Bioinformatics 31(5):647–655. https://doi.org/10.1093/bioinformatics/btu716

    Article  CAS  PubMed  Google Scholar 

  29. Christie-Oleza JA, Sousoni D, Lloyd M et al (2017) Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions. Nat Microbiol 2:17100. https://doi.org/10.1038/nmicrobiol.2017.100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Le D, Nguyen P, Nguyen D et al (2019) Gut microbiota of migrating wild rabbit fish (Siganus guttatus) larvae have low spatial and temporal variability. Microb Ecol 7:1–13. https://doi.org/10.1007/s00248-019-01436-1

    Article  CAS  Google Scholar 

  31. Miyake S, Ngugi DK, Stingl U (2015) Diet strongly influences the gut microbiota of surgeonfishes. Mol Ecol 24(3):656–672. https://doi.org/10.1111/mec.13050

    Article  PubMed  Google Scholar 

  32. Nielsen S, Walburn JW, Vergés A et al (2017) Microbiome patterns across the gastrointestinal tract of the rabbitfish Siganus fuscescens. PeerJ 5(5):3317. https://doi.org/10.7717/peerj.3317

    Article  CAS  Google Scholar 

  33. Gajardo K, Rodiles A, Kortner T et al (2016) A high-resolution map of the gut microbiota in Atlantic salmon (Salmo salar): a basis for comparative gut microbial research. Sci Rep 6:30893. https://doi.org/10.1038/srep30893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wu S, Wang G, Angert ER et al (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One 7(2):e30440. https://doi.org/10.1371/journal.pone.0030440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hills RD, Pontefract BA, Mishcon HR et al (2019) Gut microbiome: profound implications for diet and disease. Nutrients 11(7):1613. https://doi.org/10.3390/nu11071613

    Article  CAS  PubMed Central  Google Scholar 

  36. Kartzinel TR, Hsing JC, Musili PM et al (2019) Covariation of diet and gut microbiome in African megafauna. PNAS 116(47):23588–23593. https://doi.org/10.1073/pnas.1905666116

    Article  CAS  PubMed  Google Scholar 

  37. Gill SR, Pop M, Deboy R et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359. https://doi.org/10.1126/science.1124234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124(4):837–848. https://doi.org/10.1016/j.cell.2006.02.017

    Article  CAS  PubMed  Google Scholar 

  39. Luo Y, Chen H, Yu B et al (2018) Dietary pea fibre alters the microbial community and fermentation with increase in fibre degradation-associated bacterial groups in the colon of pigs. J Anim Physiol Anim Nutr (Berl) 102(1):254–261. https://doi.org/10.1111/jpn.12736

    Article  CAS  Google Scholar 

  40. Bäckhed F, Ding H, Wang T et al (2004) The gut microbiota as an environmental factor that regulates fat storage. PNAS 101(44):15718–15723. https://doi.org/10.1073/pnas.0407076101

    Article  CAS  PubMed  Google Scholar 

  41. Flint HJ, Scott KP, Duncan SH et al (2012) Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3(4):289–306. https://doi.org/10.4161/gmic.19897

    Article  PubMed  PubMed Central  Google Scholar 

  42. Tropini C, Earle KA, Huang KC et al (2017) The gut microbiome: connecting spatial organization to function. Cell Host Microbe 21(4):433–442. https://doi.org/10.1016/j.chom.2017.03.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Gu S, Chen D, Zhang JN et al (2013) Bacterial community mapping of the mouse gastrointestinal tract. PLoS One 8(10):e74957. https://doi.org/10.1371/journal.pone.0074957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Tao S, Wang JX, Liu XZ et al (2013) Preliminary research on bacterial community structure and diversity in digestive tract of Miichthys miiuy. South China Fish Sci 9(4):8–15. https://doi.org/10.3969/j.issn.2095-0780.2013.04.002

    Article  Google Scholar 

  45. Morrison M, Pope PB, Denman SE et al (2009) Plant biomass degradation by gut microbiomes: more of the same or something new? Curr Opin Biotechnol 20(3):358–363. https://doi.org/10.1016/j.copbio.2009.05.004

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Yan Xu would like to thank Tao Peng, Jidong Gu, Hui Wang, and Yirui Wu for their assistance on manuscript writing. We would like to thank EditSprings (https://www.editsprings.com/) for providing linguistic assistance during the preparation of this manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (No. 41476150), the Major University Research Foundation of Guangdong Province of China (No. 2018KCXTD012), the Science and Technology Project of Guangdong Province (2017A020217004 and 2017A040403011), and a university topic (2017KJZ01 and 2019GKTSCX071).

Author information

Author notes

  1. Yan Xu and Jin Li contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, Shantou University, No. 243, Daxue Road, Shantou, 515063, Guangdong, China

    Yan Xu, Jin Li, Xuefeng Han, Zhibiao Zhang, Mingqi Zhong & Zhong Hu

  2. Heyuan Polytechnic, Heyuan, 517000, Guangdong, China

    Yan Xu

  3. Guangdong Province Key Laboratory of Marin Biotechnology, Shantou, 515063, Guangdong, China

    Zhong Hu

Authors
  1. Yan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuefeng Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhibiao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mingqi Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhong Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZH, YX, JL, XH, and ZZ conceived the study, YX, XH, and ZZ collected samples and contributed to data analyses. YX wrote the manuscript.

Corresponding authors

Correspondence to Mingqi Zhong or Zhong Hu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 396 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Y., Li, J., Han, X. et al. Enteromorpha prolifera Diet Drives Intestinal Microbiome Composition in Siganus oramin. Curr Microbiol 78, 229–237 (2021). https://doi.org/10.1007/s00284-020-02218-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-02218-6

Search

Navigation