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Compositional and functional features of the gut microbiota of the intertidal snail Nerita yoldii along China's coast

Published online by Cambridge University Press:  18 April 2022

Ya-Jie Zhu
Affiliation:
The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao 266003, PR China
Ming-Ling Liao*
Affiliation:
The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao 266003, PR China
Meng-Wen Ding
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Marine and Earth Sciences, Xiamen University, Xiamen 361000, PR China
Zhao-Kai Wang
Affiliation:
Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, China
Yun-Wei Dong*
Affiliation:
The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao 266003, PR China Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266235, PR China
*
Author for correspondence: Ming-ling Liao, E-mail: liaoml@ouc.edu.cn; Yun-Wei Dong, E-mail: dongyw@ouc.edu.cn
Author for correspondence: Ming-ling Liao, E-mail: liaoml@ouc.edu.cn; Yun-Wei Dong, E-mail: dongyw@ouc.edu.cn

Abstract

The gut microbiota plays an important role in animals’ survival in their local environments. The intertidal rocky shore is a key interface of oceanic, atmospheric and terrestrial environments, and the transmission modes of microbes between an intertidal host and the environment are complex and largely ignored. In the present study, we characterized the gut microbiota of the intertidal snail Nerita yoldii, which is experiencing a northward range shift under the combined impacts of climate change and anthropogenic seascape transformation, and also determined the nearby environmental microbiota on the rock and in the seawater at five locations along the snail's distribution range in China. The gut microbial communities were significantly different from the environmental microbial communities, and the dominant phyla were Tenericutes, Cyanobacteria and Bacteroidetes, and Proteobacteria in the gut, rock and seawater microbial communities, respectively. At the genus level, Mycoplasma, with a relative abundance of 48.0 ± 10.2%, was the dominant genus in the gut microbial community, however, the relative abundances of this genus on the rock and in the water were low. These results imply that the gut microbial community of the intertidal snail N. yoldii is relatively independent from the environmental microbial community, and the dominant genus Mycoplasma in the gut, that is rare in the environment, can potentially assist the snail living in the harsh intertidal environment, especially at its northernmost distribution range edge.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Allison, LP, Paula, JL, Jim, RE and John, DR (2005) Climate change and distribution shifts in marine fishes. Science (New York, N.Y.) 308, 19121915.Google Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological) 57, 289300.Google Scholar
Berge, J, Johnsen, G, Nilsen, F, Gulliksen, B and Slagstad, D (2005) Ocean temperature oscillations enable reappearance of blue mussels Mytilus edulis in Svalbard after a 1000 year absence. Marine Ecology Progress Series 303, 167175.CrossRefGoogle Scholar
Bokulich, NA, Kaehler, BD, Rideout, JR, Dillon, M, Bolyen, E, Knight, R, Huttley, GA and Caporaso, JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin. Microbiome 6, 90.CrossRefGoogle ScholarPubMed
Bolyen, E, Rideout, JR, Dillon, MR, Bokulich, NA, Abnet, CC, Al-Ghalith, GA, Alexander, H, Alm, EJ, Arumugam, M, Asnicar, F, Bai, Y, Bisanz, JE, Bittinger, K, Brejnrod, A, Brislawn, CJ, Brown, CT, Callahan, BJ, Caraballo-Rodríguez, AM, Chase, J, Cope, EK, Da Silva, R, Diener, C, Dorrestein, PC, Douglas, GM, Durall, DM, Duvallet, C, Edwardson, CF, Ernst, M, Estaki, M, Fouquier, J, Gauglitz, JM, Gibbons, SM, Gibson, DL, Gonzalez, A, Gorlick, K, Guo, J, Hillmann, B, Holmes, S, Holste, H, Huttenhower, C, Huttley, GA, Janssen, S, Jarmusch, AK, Jiang, L, Kaehler, BD, Kang, KB, Keefe, CR, Keim, P, Kelley, ST, Knights, D, Koester, I, Kosciolek, T, Kreps, J, Langille, MGI, Lee, J, Ley, R, Liu, YX, Loftfield, E, Lozupone, C, Maher, M, Marotz, C, Martin, BD, McDonald, D, McIver, LJ, Melnik, AV, Metcalf, JL, Morgan, SC, Morton, JT, Naimey, AT, Navas-Molina, JA, Nothias, LF, Orchanian, SB, Pearson, T, Peoples, SL, Petras, D, Preuss, ML, Pruesse, E, Rasmussen, LB, Rivers, A, Robeson, MS 2nd, Rosenthal, P, Segata, N, Shaffer, M, Shiffer, A, Sinha, R, Song, SJ, Spear, JR, Swafford, AD, Thompson, LR, Torres, PJ, Trinh, P, Tripathi, A, Turnbaugh, PJ, Ul-Hasan, S, van der Hooft, JJJ, Vargas, F, Vázquez-Baeza, Y, Vogtmann, E, von Hippel, M, Walters, W, Wan, Y, Wang, M, Warren, J, Weber, KC, Williamson, CHD, Willis, AD, Xu, ZZ, Zaneveld, JR, Zhang, Y, Zhu, Q, Knight, R and Caporaso, JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852857.CrossRefGoogle ScholarPubMed
Burrows, MT, Hawkins, SJ, Moore, JJ, Adams, L, Sugden, H, Firth, L and Mieszkowska, N (2020) Global-scale species distributions predict temperature-related changes in species composition of rocky shore communities in Britain. Global Change Biology 26, 20932105.CrossRefGoogle Scholar
Callahan, BJ, McMurdie, PJ, Rosen, MJ, Han, AW, Johnson, AJ and Holmes, SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581583.CrossRefGoogle ScholarPubMed
Caporaso, JG, Lauber, CL, Walters, WA, Berg-Lyons, D, Huntley, J, Fierer, N, Owens, SM, Betley, J, Fraser, L, Bauer, M, Gormley, N, Gilbert, JA, Smith, G and Knight, R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6, 16211624.CrossRefGoogle ScholarPubMed
Carmody, RN, Gerber, GK, Luevano, JM Jr., Gatti, DM, Somes, L, Svenson, KL and Turnbaugh, PJ (2015) Diet dominates host genotype in shaping the murine gut microbiota. Cell Host & Microbe 17, 7284.CrossRefGoogle ScholarPubMed
Chevalier, C, Stojanović, O, Colin, DJ, Suarez-Zamorano, N, Tarallo, V, Veyrat-Durebex, C, Rigo, D, Fabbiano, S, Stevanović, A, Hagemann, S, Montet, X, Seimbille, Y, Zamboni, N, Hapfelmeier, S and Trajkovski, M (2015) Gut microbiota orchestrates energy homeostasis during cold. Cell 163, 13601374.CrossRefGoogle ScholarPubMed
Costello, EK, Stagaman, K, Dethlefsen, L, Bohannan, BJM and Relman, DA (2012) The application of ecological theory toward an understanding of the human microbiome. Science (New York, N.Y.) 336, 12551262.CrossRefGoogle ScholarPubMed
Dill-McFarland, K, Peery, M, Pauli, J and Suen, G (2015) Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths. Environmental Microbiology 18, 13911402.CrossRefGoogle ScholarPubMed
Ding, MW, Wang, ZK and Dong, YW (2018) Food availability on the shore: linking epilithic and planktonic microalgae to the food ingested by two intertidal gastropods. Marine Environmental Research 136, 7177.CrossRefGoogle Scholar
Dong, YW, Huang, XW, Wang, W, Li, Y and Wang, J (2016) The marine ‘great wall’ of China: local- and broad-scale ecological impacts of coastal infrastructure on intertidal macrobenthic communities. Diversity and Distributions 22, 731744.CrossRefGoogle Scholar
Fontaine, SS, Novarro, AJ and Kohl, KD (2018) Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian. Journal of Experimental Biology 221, jeb187559.CrossRefGoogle ScholarPubMed
Hakim, JA, Koo, H, Kumar, R, Lefkowitz, EJ, Morrow, CD, Powell, ML, Watts, SA and Bej, AK (2016) The gut microbiome of the sea urchin, Lytechinus variegatus, from its natural habitat demonstrates selective attributes of microbial taxa and predictive metabolic profiles. FEMS Microbiology Ecology 92, fiw146.CrossRefGoogle ScholarPubMed
Hawkins, S, Watson, D, Hill, A, Harding, S, Kyriakides, M, Hutchinson, S and Norton, TA (1989) A comparison of feeding mechanisms in microphagous, herbivorous, intertidal, prosobranchs in relation to resource partitioning. Journal of Molluscan Studies 55, 151165.CrossRefGoogle Scholar
Helmuth, B, Mieszkowska, N, Moore, P and Hawkins, SJ (2006) Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annual Review of Ecology, Evolution and Systematics 37, 373404.CrossRefGoogle Scholar
Huey, RB, Kearney, MR, Krockenberger, A, Holtum, JA, Jess, M and Williams, SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B 367, 16651679.CrossRefGoogle ScholarPubMed
Katoh, K, Misawa, K, Kuma, KI and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 30593066.CrossRefGoogle ScholarPubMed
Li, H, Li, TT, Yao, MJ, Li, JB, Zhang, SH, Wirth, S, Cao, WD, Lin, Q and Li, XZ (2016) Pika gut may select for rare but diverse environmental bacteria. Frontiers in Microbiology 7, 1269.CrossRefGoogle ScholarPubMed
Li, L, Xue, CH, Zhang, TT and Wang, YM (2020) The interaction between dietary marine components and intestinal flora. Marine Life Science & Technology 2, 161171.CrossRefGoogle Scholar
Liao, ML, Li, GY, Wang, J, Marshall, DJ, Hui, TY, Ma, SY, Zhang, YM, Helmuth, B and Dong, YW (2021) Physiological determinants of biogeography: the importance of metabolic depression to heat tolerance. Global Change Biology 27, 25612579.CrossRefGoogle ScholarPubMed
Lokmer, A, Kuenzel, S, Baines, JF and Wegner, KM (2016) The role of tissue-specific microbiota in initial establishment success of Pacific oysters. Environmental Microbiology 18, 970987.CrossRefGoogle ScholarPubMed
Lozupone, C and Knight, R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71, 82288235.CrossRefGoogle ScholarPubMed
Lozupone, CA, Hamady, M, Kelley, ST and Knight, R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Applied and Environmental Microbiology 73, 15761585.CrossRefGoogle ScholarPubMed
Ma, L, Zhang, QB, Yang, CF, Zhu, YG, Zhang, LP, Wang, LJ, Liu, ZW, Zhang, GT and Zhang, CS (2020) Assembly line and post-PKS modifications in the biosynthesis of marine polyketide natural products. In Liu, H-W and Begley, TP (eds), Comprehensive Natural Products III. Oxford: Elsevier, pp. 139197.CrossRefGoogle Scholar
McDonald, D, Price, MN, Goodrich, J, Nawrocki, EP, DeSantis, TZ, Probst, A, Andersen, GL, Knight, R and Hugenholtz, P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. The ISME Journal 6, 610618.CrossRefGoogle ScholarPubMed
Norton, TA, Hawkins, SJ, Manley, NL, Williams, GA and Watson, DC (1990) Scraping a living: a review of littorinid grazing. Hydrobiologia 193, 117138.CrossRefGoogle Scholar
Ng, SH, Stat, M, Bunce, M and Simmons, LW (2018) The influence of diet and environment on the gut microbial community of field crickets. Ecology and Evolution 8, 47044720.CrossRefGoogle ScholarPubMed
Offret, C, Paulino, S, Gauthier, O, Château, K, Bidault, A, Corporeau, C, Miner, P, Petton, B, Pernet, F, Fabioux, C, Paillard, C and Blay, GL (2020) The marine intertidal zone shapes oyster and clam digestive bacterial microbiota. FEMS Microbiology Ecology 96, fiaa078.CrossRefGoogle ScholarPubMed
Parks, DH, Tyson, GW, Hugenholtz, P and Beiko, RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics (Oxford, England) 30, 31233124.CrossRefGoogle Scholar
Price, MN, Dehal, PS and Arkin, AP (2010) FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490.CrossRefGoogle ScholarPubMed
Rude, MA and Khosla, C (2006) Production of ansamycin polyketide precursors in Escherichia coli. Journal of Antibiotics 59, 464470.CrossRefGoogle ScholarPubMed
Sirami, C, Caplat, P, Popy, S, Clamens, A, Arlettaz, R, Jiguet, F, Brotons, L and Martin, J-L (2017) Impacts of global change on species distributions: obstacles and solutions to integrate climate and land use. Global Ecology and Biogeography 26, 385394.CrossRefGoogle Scholar
Somero, GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. Journal of Experimental Biology 213, 912920.CrossRefGoogle Scholar
Somero, GN, Lockwood, B and Tomanek, L (2017) Biochemical Adaptation: Response to Environmental Challenges, from Life's Origins to the Anthropocene. Sunderland, MA: Sinauer Associates.Google Scholar
Soriano, EL, Ramírez, DT, Araujo, DR, Gómez-Gil, B, Castro, LI and Sánchez, CG (2018) Effect of temperature and dietary lipid proportion on gut microbiota in yellowtail kingfish Seriola lalandi juveniles. Aquaculture 497, 269277.CrossRefGoogle Scholar
Stillman, JH and Somero, GN (1996) Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus Petrolisthes): correlation of physiology, biochemistry and morphology with vertical distribution. Journal of Experimental Biology 199, 18451855.CrossRefGoogle ScholarPubMed
Sylvain, FE, Cheaib, B, Llewellyn, M, Gabriel Correia, T, Barros Fagundes, D, Luis Val, A and Derome, N (2016) pH drop impacts differentially skin and gut microbiota of the Amazonian fish tambaqui (Colossoma macropomum). Scientific Reports 6, 32032.CrossRefGoogle Scholar
Tong, YR and Meng, WX (1985) Studies on molluscan fauna of Jiangsu coastal sea. Journal of Nanjing University (Natural Sciences Edition) 1, 111119. [In Chinese, with English abstract.]Google Scholar
VanDerWal, J, Murphy, HT, Kutt, AS, Perkins, GC, Bateman, BL, Perry, JJ and Reside, AE (2012) Focus on poleward shifts in species' distribution underestimates the fingerprint of climate change. Nature Climate Change 3, 239243.CrossRefGoogle Scholar
Vellend, BM (2010) Conceptual synthesis in community ecology. Quarterly Review of Biology 85, 183206.CrossRefGoogle ScholarPubMed
Wang, J, Yan, HY, Cheng, ZY, Huang, XW, Wang, W, Ding, MW and Dong, YW (2018) Recent northward range extension of Nerita yoldii (Gastropoda: Neritidae) on artificial rocky shores in China. Journal of Molluscan Studies 84, 345353.Google Scholar
Wang, W, Wang, J, Choi, FMP, Ding, P, Li, XX, Han, GD, Ding, MW, Guo, M, Huang, XW, Duan, WX, Cheng, ZY, Chen, ZY, Hawkins, SJ, Jiang, Y, Helmuth, B and Dong, YW (2020) Global warming and artificial shorelines reshape seashore biogeography. Global Ecology and Biogeography 29, 220231.CrossRefGoogle Scholar
Welch, BL (1938) The significance of the difference between two means when the population variances are unequal. Biometrika 29, 350362.CrossRefGoogle Scholar
Whitesell, L, Shifrin, S, Schwab, G and Neckers, L (1992) Benzoquinonoid ansamycins possess selective tumoricidal activity unrelated to src kinase inhibition. Cancer Research 52, 17211728.Google ScholarPubMed
Wong, S and Rawls, JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Molecular Ecology 21, 31003102.CrossRefGoogle ScholarPubMed
Zacherl, D, Gaines, SD and Lonhart, SI (2003) The limits to biogeographical distributions: insights from the northward range extension of the marine snail, Kelletia kelletii (Forbes, 1852). Journal of Biogeography 30, 913924.CrossRefGoogle Scholar
Zhang, H and Lin, SJ (2005) Development of a cob-18S rRNA gene real-time PCR assay for quantifying Pfiesteria shumwayae in the nature environment. Applied and Environmental Microbiology 71, 70537063.CrossRefGoogle Scholar
Zhang, W, Li, N, Tang, X, Liu, N and Zhao, W (2018) Changes in intestinal microbiota across an altitudinal gradient in the lizard Phrynocephalus vlangalii. Ecology and Evolution 8, 46954703.CrossRefGoogle ScholarPubMed
Zhang, Y, Liang, XF, He, S, Chen, X, Wang, J, Li, J, Zhu, Q, Zhang, Z, Li, L and Alam, MS (2020) Effects of high carbohydrate diet-modulated microbiota on gut health in Chinese perch. Frontiers in Microbiology 11, 2255.Google ScholarPubMed

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Compositional and functional features of the gut microbiota of the intertidal snail Nerita yoldii along China's coast
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