Enrichment of Bacteria and Alginate Lyase Genes Potentially Involved in Brown Alga Degradation in the Gut of Marine Gastropods

Overview

Journal Sci Rep

Specialty Science

Date 2019 Feb 16

PMID 30765748

Citations 10

Authors

Michihiro Ito

Kotaro Watanabe

Toru Maruyama

Tetsushi Mori

Kentaro Niwa

Seinen Chow

Haruko Takeyama

Affiliations

Soon will be listed here.

Abstract

Gut bacteria of phytophagous and omnivorous marine invertebrates often possess alginate lyases (ALGs), which are key enzymes for utilizing macroalgae as carbon neutral biomass. We hypothesized that the exclusive feeding of a target alga to marine invertebrates would shift the gut bacterial diversity suitable for degrading the algal components. To test this hypothesis, we reared sea hare (Dolabella auricularia) and sea snail (Batillus cornutus) for two to four weeks with exclusive feeding of a brown alga (Ecklonia cava). Pyrosequencing analysis of the gut bacterial 16S rRNA genes revealed shifts in the gut microbiota after rearing, mainly due to a decrease in the variety of bacterial members. Significant increases in six and four 16S rRNA gene phylotypes were observed in the reared sea hares and sea snails, respectively, and some of them were phylogenetically close to known alginate-degrading bacteria. Clone library analysis of PL7 family ALG genes using newly designed degenerate primer sets detected a total of 50 ALG gene phylotypes based on 90% amino acid identity. The number of ALG gene phylotypes increased in the reared sea hare but decreased in reared sea snail samples, and no phylotype was shared between them. Out of the 50 phylotypes, 15 were detected only after the feeding procedure. Thus, controlled feeding strategy may be valid and useful for the efficient screening of genes suitable for target alga fermentation.

Citing Articles

Gut microbiota in parasite-transmitting gastropods.

Li P, Hong J, Yuan Z, Huang Y, Wu M, Ding T Infect Dis Poverty. 2023; 12(1):105.

PMID: 38001502 PMC: 10668521. DOI: 10.1186/s40249-023-01159-z.

Chitinolytic and Fungicidal Potential of the Marine Bacterial Strains Habituating Pacific Ocean Regions.

Pentekhina I, Nedashkovskaya O, Seitkalieva A, Gorbach V, Slepchenko L, Kirichuk N Microorganisms. 2023; 11(9).

PMID: 37764100 PMC: 10535946. DOI: 10.3390/microorganisms11092255.

Gut Microbiota of Freshwater Gastropod () Assist the Adaptation of Host to Toxic Cyanobacterial Stress.

Liu H, Yang X, Yang W, Zheng Z, Zhu J Toxins (Basel). 2023; 15(4).

PMID: 37104190 PMC: 10141019. DOI: 10.3390/toxins15040252.

Female reproductive dysfunctions and the gut microbiota.

Chadchan S, Singh V, Kommagani R J Mol Endocrinol. 2022; 69(3):R81-R94.

PMID: 35900833 PMC: 10031513. DOI: 10.1530/JME-21-0238.

Responses of Gut Microbial Community Composition and Function of the Freshwater Gastropod to Cyanobacterial Bloom.

Lyu T, Zhu J, Yang X, Yang W, Zheng Z Front Microbiol. 2022; 13:906278.

PMID: 35633671 PMC: 9136413. DOI: 10.3389/fmicb.2022.906278.

References

Sugimura I , Sawabe , Ezura . Cloning and Sequence Analysis of Vibrio halioticoli Genes Encoding Three Types of Polyguluronate Lyase. Mar Biotechnol (NY). 2000; 2(1):65-73. DOI: 10.1007/s101269900010. View

Wong T, Preston L, Schiller N . ALGINATE LYASE: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol. 2000; 54:289-340. DOI: 10.1146/annurev.micro.54.1.289. View

Katoh K, Misawa K, Kuma K, Miyata T . MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14):3059-66. PMC: 135756. DOI: 10.1093/nar/gkf436. View

Kawasaki K, Nogi Y, Hishinuma M, Nodasaka Y, Matsuyama H, Yumoto I . Psychromonas marina sp. nov., a novel halophilic, facultatively psychrophilic bacterium isolated from the coast of the Okhotsk Sea. Int J Syst Evol Microbiol. 2002; 52(Pt 5):1455-1459. DOI: 10.1099/00207713-52-5-1455. View

Ohkuma M . Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol. 2003; 61(1):1-9. DOI: 10.1007/s00253-002-1189-z. View

Hayashi K, Moriwaki J, Sawabe T, Thompson F, Swings J, Gudkovs N . Vibrio superstes sp. nov., isolated from the gut of Australian abalones Haliotis laevigata and Haliotis rubra. Int J Syst Evol Microbiol. 2003; 53(Pt 6):1813-7. DOI: 10.1099/ijs.0.02625-0. View

Sawabe T, Hayashi K, Moriwaki J, Fukui Y, Thompson F, Swings J . Vibrio neonatus sp. nov. and Vibrio ezurae sp. nov. isolated from the gut of Japanese abalones. Syst Appl Microbiol. 2004; 27(5):527-34. DOI: 10.1078/0723202041748154. View

Ochiai A, Hashimoto W, Murata K . A biosystem for alginate metabolism in Agrobacterium tumefaciens strain C58: molecular identification of Atu3025 as an exotype family PL-15 alginate lyase. Res Microbiol. 2006; 157(7):642-9. DOI: 10.1016/j.resmic.2006.02.006. View

Kawamoto H, Horibe A, Miki Y, Kimura T, Tanaka K, Nakagawa T . Cloning and sequencing analysis of alginate lyase genes from the marine bacterium Vibrio sp. O2. Mar Biotechnol (NY). 2006; 8(5):481-90. DOI: 10.1007/s10126-005-6157-z. View

10.

Sawabe T, Fujimura Y, Niwa K, Aono H . Vibrio comitans sp. nov., Vibrio rarus sp. nov. and Vibrio inusitatus sp. nov., from the gut of the abalones Haliotis discus discus, H. gigantea, H. madaka and H. rufescens. Int J Syst Evol Microbiol. 2007; 57(Pt 5):916-922. DOI: 10.1099/ijs.0.64789-0. View

11.

Hayashi A, Aoyagi H, Yoshimura T, Tanaka H . Development of novel method for screening microorganisms using symbiotic association between insect (Coptotermes formosanus Shiraki) and intestinal microorganisms. J Biosci Bioeng. 2007; 103(4):358-67. DOI: 10.1263/jbb.103.358. View

12.

Ogura K, Yamasaki M, Mikami B, Hashimoto W, Murata K . Substrate recognition by family 7 alginate lyase from Sphingomonas sp. A1. J Mol Biol. 2008; 380(2):373-85. DOI: 10.1016/j.jmb.2008.05.008. View

13.

Cantarel B, Coutinho P, Rancurel C, Bernard T, Lombard V, Henrissat B . The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2008; 37(Database issue):D233-8. PMC: 2686590. DOI: 10.1093/nar/gkn663. View

14.

Hamady M, Lozupone C, Knight R . Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 2009; 4(1):17-27. PMC: 2797552. DOI: 10.1038/ismej.2009.97. View

15.

Uchimura K, Miyazaki M, Nogi Y, Kobayashi T, Horikoshi K . Cloning and sequencing of alginate lyase genes from deep-sea strains of Vibrio and Agarivorans and characterization of a new Vibrio enzyme. Mar Biotechnol (NY). 2009; 12(5):526-33. DOI: 10.1007/s10126-009-9237-7. View

16.

Lozupone C, Lladser M, Knights D, Stombaugh J, Knight R . UniFrac: an effective distance metric for microbial community comparison. ISME J. 2010; 5(2):169-72. PMC: 3105689. DOI: 10.1038/ismej.2010.133. View

17.

Bugg T, Ahmad M, Hardiman E, Singh R . The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol. 2010; 22(3):394-400. DOI: 10.1016/j.copbio.2010.10.009. View

18.

Park H, Kam N, Lee E, Kim H . Cloning and characterization of a novel oligoalginate lyase from a newly isolated bacterium Sphingomonas sp. MJ-3. Mar Biotechnol (NY). 2011; 14(2):189-202. DOI: 10.1007/s10126-011-9402-7. View

19.

Wargacki A, Leonard E, Win M, Regitsky D, Santos C, Kim P . An engineered microbial platform for direct biofuel production from brown macroalgae. Science. 2012; 335(6066):308-13. DOI: 10.1126/science.1214547. View

20.

Fernandez-Piquer J, Bowman J, Ross T, Tamplin M . Molecular analysis of the bacterial communities in the live Pacific oyster (Crassostrea gigas) and the influence of postharvest temperature on its structure. J Appl Microbiol. 2012; 112(6):1134-43. DOI: 10.1111/j.1365-2672.2012.05287.x. View