Seasonal changes in gut microbiota of sea cucumber over natural aestivation cycle

Ye ZHAO; Han WANG; Haona WANG; Lijie ZHANG; Hao SUN; Yanying ZHANG

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Seasonal changes in gut microbiota of sea cucumber over natural aestivation cycle

Ecology | Updated：2024-10-14

- Seasonal changes in gut microbiota of sea cucumber over natural aestivation cycle
- Journal of Oceanology and Limnology Vol. 42, Issue 3, Pages: 849-864(2024)
- Affiliations：
  
  Ocean School, Yantai University, Yantai 264005, China
- Author bio：
  
  zyzy19872006@163.com
  zhyanying@163.com
- Funds：
- DOI：
  CLC：
- Received：26 April 2023，
  
  Accepted：05 June 2023，
  
  Online First：08 August 2023，
  
  Published：01 May 2024
- Accepted：
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ZHAO Ye,WANG Han,WANG Haona,et al.Seasonal changes in gut microbiota of sea cucumber over natural aestivation cycle[J].Journal of Oceanology and Limnology,2024,42(03):849-864.
DOI：

ZHAO Ye,WANG Han,WANG Haona,et al.Seasonal changes in gut microbiota of sea cucumber over natural aestivation cycle[J].Journal of Oceanology and Limnology,2024,42(03):849-864. DOI：

摘要

Abstract

Sea cucumber

Apostichopus

japonicus

is an ideal model organism for marine invertebrate aestivation; it annually enters a “s

leeping state” for nearly 3 months when ambient water temperature range is 25–30 °‍‍C. The natural fasting is accompanied by remodeling the intestinal biota and function

which is a part of host biology and could affect the gut microbiota. We investigatesd the impact of annual aestivation on gut microbiota using high-throughput sequencing of 16S rRNA amplicons. Results reveal a notable alteration in the composition of gut bacteria during aestivation during which various indigenous families and genera that exhibit a preference for dietary glycans (e.g.

family Rhodobacteraceae and Flavobacteriaceae) decreased

while the taxa capable of utilizing substrates derived from the host (e.g.

genus

Akkermansia

and

Prevotella

) increased

and so did certain opportunistic pathogenic bacteria. Moreover

the investigation delved into the gut morphology and immunity response of

japonicus

and reveal that the intestine of

japonicus

undergoes substantial atrophy and degeneration during aestivation. However

there was an observed augmentation in the levels of acid and neutral mucin within mucous cells

as well as an enhanced immune defense response (as evidenced by increased gene expression of

AjTLR3

LITAF

Ajp105

and

LYZ

). These results imply that the composition of sea cucumber gut microbiota differed between aestivation and active periods

which potentially affects the intestinal functions of the host and the symbiotic relationship between host and its microbiota over the active-aestivation cycle.

关键词

Keywords

references

Achbergerová L , Nahálka J . 2014 . Degradation of polyphosphates by polyphosphate kinases from Ruegeria pomeroyi . Biotechnology Letters , 36 ( 10 ): 2029 - 2035 , https://doi.org/10.1007/s10529-014-1566-6 https://doi.org/10.1007/s10529-014-1566-6 .

Agus A , Clément K , Sokol H . 2021 . Gut microbiota-derived metabolites as central regulators in metabolic disorders . Gut , 70 ( 6 ): 1174 - 1182 , https://doi.org/10.1136/gutjnl-2020-323071 https://doi.org/10.1136/gutjnl-2020-323071 .

Bäckhed F , Ley R E , Sonnenburg J L et al . 2005 . Host-bacterial mutualism in the human intestine . Science , 307 ( 5717 ): 1915 - 1920 , https://doi.org/10.1126/science.1104816 https://doi.org/10.1126/science.1104816 .

Banas J A , Loesche W J , Nace G W . 1988 . Possible mechanisms responsible for the reduced intestinal flora in hibernating leopard frogs ( Rana pipiens ) . Applied and Environmental Microbiology , 54 ( 9 ): 2311 - 2317 , https://doi.org/10.1128/aem.54.9.2311-2317.1988 https://doi.org/10.1128/aem.54.9.2311-2317.1988 .

Barnes E M , Burton G C . 1970 . The effect of hibernation on the caecal flora of the thirteen-lined ground squirrel ( Citellus tridecemlineatus ) . Journal of Applied Bacteriology , 33 ( 3 ): 505 - 514 , https://doi.org/10.1111/j.1365-2672.1970.tb02227.x https://doi.org/10.1111/j.1365-2672.1970.tb02227.x .

Cant J P , McBride B W , Jr Croom W J . 1996 . The regulation of intestinal metabolism and its impact on whole animal energetics . Journal of Animal Science , 74 ( 10 ): 2541 - 2553 , https://doi.org/10.2527/1996.74102541x https://doi.org/10.2527/1996.74102541x .

Carey H V . 1990 . Seasonal changes in mucosal structure and function in ground squirrel intestine . American Journal of Physiology-Regulatory, Integrative and Comparative Physiology , 259 ( 2 ): R385 - R392 , https://doi.org/10.1152/ajpregu.1990.259.2.R385 https://doi.org/10.1152/ajpregu.1990.259.2.R385 .

Carey H V , Assadi-Porter F M . 2017 . The hibernator microbiome: host-bacterial interactions in an extreme nutritional symbiosis . Annual Review of Nutrition , 37 : 477 - 500 , https://doi.org/10.1146/annurev-nutr-071816-064740 https://doi.org/10.1146/annurev-nutr-071816-064740 .

Carey H V , Walters W A , Knight R . 2013 . Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle . American Journal of Physiology-Regulatory, Integrative and Comparative Physiology , 304 ( 1 ): R33 - R42 , https://doi.org/10.1152/ajpregu.00387.2012 https://doi.org/10.1152/ajpregu.00387.2012 .

Chen M Y , Wang S S , Li X K et al . 2018 . The potential contribution of miRNA-200-3p to the fatty acid metabolism by regulating AjEHHADH during aestivation in sea cucumber . PeerJ , 6 : e5703 , https://doi.org/10.7717/peerj.5703 https://doi.org/10.7717/peerj.5703 .

Cramp R L , Franklin C E . 2005 . Arousal and re-feeding rapidly restores digestive tract morphology following aestivation in green-striped burrowing frogs . Comparative Biochemistry and Physiology Part A : Molecular & Integrative Physiology , 142 ( 4 ): 451 - 460 , https://doi.org/10.1016/j.cbpa.2005.09.013 https://doi.org/10.1016/j.cbpa.2005.09.013 .

David L A , Maurice C F , Carmody R N et al . 2014 . Diet rapidly and reproducibly alters the human gut microbiome . Nature , 505 ( 7484 ): 559 - 563 , https://doi.org/10.1038/nature12820 https://doi.org/10.1038/nature12820 .

Derrien M , Van Baarlen P , Hooiveld G et al . 2011 . Modulation of mucosal immune response, toler ance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila . Frontiers in Microbiology , 2 : 166 , https://doi.org/10.3389/fmicb.2011.00166 https://doi.org/10.3389/fmicb.2011.00166 .

Derrien M , van Passel M W J , van de Bovenkamp J H B et al . 2010 . Mucin-bacterial interactions in the human oral cavity and digestive tract . Gut Microbes , 1 ( 4 ): 254 - 268 , https://doi.org/10.4161/gmic.1.4.12778 https://doi.org/10.4161/gmic.1.4.12778 .

Derrien M , Vaughan E E , Plugge C M et al . 2004 . Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium . International Journal of Systematic and Evolutionary Microbiology , 54 ( 5 ): 1469 - 1476 , https://doi.org/10.1099/ijs.0.02873-0 https://doi.org/10.1099/ijs.0.02873-0 .

Desai M S , Seekatz A M , Koropatkin N M et al . 2016 . A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility . Cell , 167 ( 5 ): 1339 - 1353.e21 , https://doi.org/10.1016/j.cell.2016.10.043 https://doi.org/10.1016/j.cell.2016.10.043 .

Dill-McFarland K A , Neil K L , Zeng A et al . 2014 . Hibernation alters the diversity and composition of mucosa-associated bacteria while enhancing antimicrobial defence in the gut of 13-lined ground squirrels . Molecular Ecology , 23 ( 18 ): 4658 - 4669 , https://doi.org/10.1111/mec.12884 https://doi.org/10.1111/mec.12884 .

Everard A , Belzer C , Geurts L et al . 2013 . Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity . Proceedings of the National Academy of Sciences of the United States of America , 110 ( 22 ): 9066 - 9071 , https://doi.org/10.1073/pnas.1219451110 https://doi.org/10.1073/pnas.1219451110 .

Fassarella M , Blaak E E , Penders J et al . 2021 . Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health . Gut , 70 ( 3 ): 595 - 605 , http://dx.doi.org/10.1136/gutjnl-2020-321747 http://dx.doi.org/10.1136/gutjnl-2020-321747 .

Forstner G , Forstner J F . 1994 . Gastrointestinal mucus . In: Johnson L R ed. Physiology of the Gastrointestinal Tract . Raven Press , New York, USA . p. 1255 - 1283 .

Frick N T , Bystriansky J S , Ip Y K et al . 2008 . Lipid, ketone body and oxidative metabolism in the African lungfish, Protopterus dolloi following 60 days of fasting and aestivation . Comparative Biochemistry and Physiology Part A : Molecular & Integrative Physiology , 151 ( 1 ): 93 - 101 , https://doi.org/10.1016/j.cbpa.2008.06.004 https://doi.org/10.1016/j.cbpa.2008.06.004 .

Fu S Z , Fan H X , Liu S J et al . 2009 . A bioaugmentation failure caused by phage infection and weak biofilm formation ability . Journal of Environmental Sciences , 21 ( 8 ): 1153 - 1161 , https://doi.org/10.1016/S1001-0742(08)62396-7 https://doi.org/10.1016/S1001-0742(08)62396-7 .

Glavan T W , Gaulke C A , Rocha C S et al . 2016 . Gut immune dysfunction through impaired innate pattern recognition receptor expression and gut microbiota dysbiosis in chronic SIV infection . Mucosal Immunology , 9 ( 3 ): 677 - 688 , https://doi.org/10.1038/mi.2015.92 https://doi.org/10.1038/mi.2015.92 .

Guppy M , Withers P . 1999 . Metabolic depression in animals: physiological perspectives and biochemical generalizations . Biological Reviews , 74 ( 1 ): 1 - 40 , https://doi.‍org/10.1017/S0006323198005258 https://doi.‍org/10.1017/S0006323198005258 . https://do 10.1111/j.1469-185x.1999.tb00180.x http://dx.doi.org/10.1111/j.1469-185x.1999.tb00180.x

Hasan N , Yang H Y . 2019 . Factors affecting the composition of the gut microbiota, and its modulation . PeerJ , 7 : e7502 , https://doi.org/10.7717/peerj.7502 https://doi.org/10.7717/peerj.7502 .

He W Q , Rahimnejad S , Wang L et al . 2017 . Effects of organic acids and essential oils blend on growth, gut microbiota, immune response and disease resistance of Pacific white shrimp ( Litopenaeus vannamei ) against Vibrio parahaemolyticus . Fish & shellfish immunology , 70 : 164 - 173 , https://doi.org/10.1016/j.fsi.2017.09.007 https://doi.org/10.1016/j.fsi.2017.09.007 .

Hooper L V , Littman D R , Macpherson A J . 2012 . Interactions between the microbiota and the immune system . Science , 336 ( 6086 ): 1268 - 1273 , https://doi.org/10.1126/science.1223490 https://doi.org/10.1126/science.1223490 .

Jia C C , Zhu X Z , Meng X Y et al . 2020 . Effects of Jerusalem artichoke powder on the growth performance, nonspecific immunity, and gastrointestinal microbiota of sea cucumber . Journal of the World Aquaculture Society , 51 ( 1 ): 200 - 213 , https://doi.org/10.1111/jwas.12633 https://doi.org/10.1111/jwas.12633 .

Jones R M . 1980 . Metabolic consequences of accelerated urea synthesis during seasonal dormancy of spadefoot toads, Scaphiopus couchi and Scaphiopus multiplicatus . Journal of Experimental Zoology , 212 ( 2 ): 255 - 267 , https://doi.org/10.1002/jez.1402120212 https://doi.org/10.1002/jez.1402120212 .

Kang Y H , Yang B T , Hu R G et al . 2023 . Gut microbiota and metabolites may play a crucial role in sea cucumber Apostichopus japonicus aestivation . Microorganisms , 11 ( 2 ): 416 , https://doi.org/10.3390/microorganisms11020416 https://doi.org/10.3390/microorganisms11020416 .

Kashyap P C , Marcobal A , Ursell L K et al . 2013 . Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota . Proceedings of the National Academy of Sciences of the United States of America , 110 ( 42 ): 17059 - 17064 , https://doi.org/10.1073/pnas.1306070110 https://doi.org/10.1073/pnas.1306070110 .

Kurtz C C , Carey H V . 2007 . Seasonal changes in the intestinal immune system of hibernating ground squirrels . Developmental & Comparative Immunology , 31 ( 4 ): 415 - 428 , https://doi.org/10.1016/j.dci.2006.07.003 https://doi.org/10.1016/j.dci.2006.07.003 .

Li F X , Liu Y H , Song B X et al . 1996 . Study on aestivating habit of sea cucumber ( Apostichopus japonicus Selenka) II. the factors relating to aestivation . Journal of Fishery Sciences of China , 3 ( 2 ): 49 - 57 , https://kns.cnki.net/kcms2/article/abstract?v=O9dCEmDP74KUIVtMEgJ8xLSV1nOZLmXw2ZVzJrD0w34eZQT2xfO1dZADnGAi3cEiKLgXlSiU2b0Xb_Hx046SyEchG_70xcrT5dKyoAZxEfKTE52FfaUPRFPOiFqi1o1k&uniplatform=NZKPT&language=CHS. https://kns.cnki.net/kcms2/article/abstract?v=O9dCEmDP74KUIVtMEgJ8xLSV1nOZLmXw2ZVzJrD0w34eZQT2xfO1dZADnGAi3cEiKLgXlSiU2b0Xb_Hx046SyEchG_70xcrT5dKyoAZxEfKTE52FfaUPRFPOiFqi1o1k&uniplatform=NZKPT&language=CHS. (in Chinese with English abstract)

Li J , Liao M J , Li B et al . 2019 . The characteristics of culturable bacterial microflora in the gastrointestinal tract of cultured sea cucumber ( Apostichopus japonicus ) during the early developmental stage and its relationship with environmental flora . Progress in Fishery Sciences , 40 ( 2 ): 122 - 131 , https://doi.org/10.19663/j.issn2095-9869.20180406003. https://doi.org/10.19663/j.issn2095-9869.20180406003. (in Chinese with English abstract)

Ma Y X , Li L Y , Li M et al . 2019 . Effects of dietary probiotic yeast on growth parameters in juvenile sea cucumber, Apostichopus japonicus . Aquaculture , 499 : 203 - 211 , https://doi.org/10.1016/j.aquaculture.2018.09.043 https://doi.org/10.1016/j.aquaculture.2018.09.043 .

Macchione I G , Lopetuso L R , Ianiro G et al . 2019 . Akkermansia muciniphila : key player in metabolic and gastrointestinal disorders . European Review for Medical and Pharmacological Sciences , 23 ( 18 ): 8075 - 8083 , https://doi.org/10.26355/eurrev_201909_19024 https://doi.org/10.26355/eurrev_201909_19024 .

Magnuson E , Mykytczuk N C S , Pellerin A et al . 2021 . Thiomicrorhabdus streamers and sulfur cycling in perennial hypersaline cold springs in the Canadian high Arctic . Environmental Microbiology , 23 ( 7 ): 3384 - 3400 , https://doi.org/10.1111/1462-2920.14916 https://doi.org/10.1111/1462-2920.14916 .

Marcobal A , Southwick A M , Earle K A et al . 2013 . A refined palate: bacterial consumption of host glycans in the gut . Glycobiology , 23 ( 9 ): 1038 - 1046 , https://doi.‍org/10.1093/glycob/cwt040 https://doi.‍org/10.1093/glycob/cwt040 . https://do 10.1093/glycob/cwt040 http://dx.doi.org/10.1093/glycob/cwt040

Marra A , Hanson M A , Kondo S et al . 2021 . Drosophila antimicrobial peptides and lysozymes regulate gut microbiota composition and abundance . mBio , 12 ( 4 ): e0082421 , https://doi.org/10.1101/2021.03.19.436153 https://doi.org/10.1101/2021.03.19.436153 .

Masschalck B , Michiels C W . 2003 . Antimicrobial properties of lysozyme in relation to foodborne vegetative bacteria . Critical Reviews in Microbiology , 29 ( 3 ): 191 - 214 , https://doi.org/10.1080/713610448 https://doi.org/10.1080/713610448 .

McFall-Ngai M , Hadfield M G , Bosch T C G et al . 2013 . Animals in a bacterial world, a new imperative for the life sciences . Proceedings of the National Academy of Sciences of the United States of America , 110 ( 9 ): 3229 - 3236 , https://doi.org/10.1073/pnas.1218525110 https://doi.org/10.1073/pnas.1218525110 .

Michielan A , D'Incà R . 2015 . Intestinal permeability in inflammatory bowel disease: pathogenesis, clinical evaluation, and therapy of leaky gut . Mediators of Inflammation , 2015 : 628157 , https://doi.org/10.1155/2015/628157 https://doi.org/10.1155/2015/628157 .

Pelaseyed T , Bergström J H , Gustafsson J K et al . 2014 . The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system . Immunological Reviews , 260 ( 1 ): 8 - 20 , https://doi.org/10.1111/imr.12182 https://doi.org/10.1111/imr.12182 .

Peng C , Ouyang Y B , Lu N H et al . 2020 . The NF-κB signaling pathway, the microbiota, and gastrointestinal tumorigenesis: recent advances . Frontiers in Immunology , 11 : 1387 , https://doi.org/10.3389/fimmu.2020.01387 https://doi.org/10.3389/fimmu.2020.01387 .

Pinder A W , Storey K B , Ultsch G R . 1992 . Estivation and hibernation . In: Feder M E, Burggren W W eds. Environmental Physiology of the Amphibians . University of Chicago Press, Chicago. p. 250 - 276 . https://do 10.2307/1447109 http://dx.doi.org/10.2307/1447109

Planas M , Pérez-Lorenzo M , Hjelm M et al . 2006 . Probiotic effect in vivo of Roseobacter strain 27 - 4 against Vibrio (Listonella) anguillarum infections in turbot (Scophthalmus maximus L.) larvae. Aquaculture , 255 ( 1-4 ): 323 - 333 , https://doi.org/10.1016/j.aquaculture.2005.11.039 https://doi.org/10.1016/j.aquaculture.2005.11.039 .

Reunanen J , Kainulainen V , Huuskonen L et al . 2015 . Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of the epithelial cell layer . Applied and Environmental Microbiology , 81 ( 11 ): 3655 - 3662 , https://doi.org/10.1128/AEM.04050-14 https://doi.org/10.1128/AEM.04050-14 .

Rosenfeld C S . 2017 . Gut dysbiosis in animals due to environmental chemical exposures . Frontiers in Cellular and Infection Microbiology , 7 : 396 , https://doi.org/10.3389/fcimb.2017.00396 https://doi.org/10.3389/fcimb.2017.00396 .

Round J L , Mazmanian S K . 2009 . The gut microbiota shapes intestinal immune responses during health and disease . Nature Reviews Immunology , 9 ( 5 ): 313 - 323 , https://doi.org/10.1038/nri2515 https://doi.org/10.1038/nri2515 .

Schoeler M , Caesar R . 2019 . Dietary lipids, gut microbiota and lipid metabolism . Reviews in Endocrine and Metabolic Disorders , 20 ( 4 ): 461 - 472 , https://doi.org/10.1007/s11154-019-09512-0 https://doi.org/10.1007/s11154-019-09512-0 .

Secor S M . 2005a . Evolutionary and cellular mechanisms regulating intestinal performance of amphibians and reptiles . Integrative and Comparative Biology , 45 ( 2 ): 282 - 294 , https://doi.org/10.1093/icb/45.2.282 https://doi.org/10.1093/icb/45.2.282 .

Secor S M . 2005b . Physiological responses to feeding, fasting and estivation for anurans . Journal of Experimental Biology , 208 ( 13 ): 2595 - 2609 , https://doi.org/10.1242/jeb.01659 https://doi.org/10.1242/jeb.01659 .

Secor S M , Diamond J . 1995 . Adaptive responses to feeding in Burmese pythons: pay before pumping . Journal of Experimental Biology , 198 ( 6 ): 1313 - 1325 , https://doi.org/10.1242/jeb.198.6.1313 https://doi.org/10.1242/jeb.198.6.1313 .

Sha Y J , Liu M , Wang B J et al . 2016 . Gut bacterial diversity of farmed sea cucumbers Apostichopus japonicus with different growth rates . Microbiology , 85 ( 1 ): 109 - 115 , https://doi.org/10.1134/S0026261716010112 https://doi.org/10.1134/S0026261716010112 .

Shi N , Li N , Duan X W et al . 2017 . Interaction between the gut microbiome and mucosal immune system . Military Medical Research , 4 ( 1 ): 14 , https://doi.org/10.1186/s40779-017-0122-9 https://doi.org/10.1186/s40779-017-0122-9 .

Singh S , Bhatia R , Singh A et al . 2018 . Probiotic attributes and prevention of LPS-induced pro-inflammatory stress in RAW264.7 macrophages and human intestinal epithelial cell line (Caco-2) by newly isolated Weissella cibaria strains . Food & Function , 9 ( 2 ): 1254 - 1264 , https://doi.org/10.1039/C7FO00469A https://doi.org/10.1039/C7FO00469A .

Sommer F , Bäckhed F . 2016 . Know your neighbor: microbiota and host epithelial cells interact locally to control intestinal function and physiology . BioEssays , 38 ( 5 ): 455 - 464 , https://doi.org/10.1002/bies.201500151 https://doi.org/10.1002/bies.201500151 .

Sonnenburg J L , Xu J , Leip D D et al . 2005 . Glycan foraging in vivo by an intestine-adapted bacterial symbiont . Science , 307 ( 5717 ): 1955 - 1959 , https://doi.‍org/10.1126/science.1109051 https://doi.‍org/10.1126/science.1109051 . https://do 10.1126/science.1109051 http://dx.doi.org/10.1126/science.1109051

Sonoyama K , Fujiwara R , Takemura N et al . 2009 . Response of gut microbiota to fasting and hibernation in Syrian hamsters . Applied and Environmental Microbiology , 75 ( 20 ): 6451 - 6456 , https://doi.org/10.1128/AEM.00692-09 https://doi.org/10.1128/AEM.00692-09 .

Starck J M , Cruz-Neto A P , Abe A S . 2007 . Physiological and morphological responses to feeding in broad-nosed caiman ( Caiman latirostris ) . Journal of Experimental Biology , 210 ( 12 ): 2033 - 2045 , https://doi.org/10.1242/jeb.000976 https://doi.org/10.1242/jeb.000976 .

Stevenson T J , Duddleston K N , Buck C L . 2014 . Effects of season and host physiological state on the diversity, density, and activity of the arctic ground squirrel cecal microbiota . Applied and Environmental Microbiology , 80 ( 18 ): 5611 - 5622 , https://doi.org/10.1128/AEM.01537-14 https://doi.org/10.1128/AEM.01537-14 .

Storey K B . 2002 . Life in the slow lane: molecular mechanisms of estivation . Comparative Biochemistry and Physiology Part A : Molecular & Integrative Physiology , 133 ( 3 ): 733 - 754 , https://doi.org/10.1016/S1095-6433(02)00206-4 https://doi.org/10.1016/S1095-6433(02)00206-4 .

Sun H J , Zhou Z C , Dong Y et al . 2013 . Identification and expression analysis of two Toll-like receptor genes from sea cucumber ( Apostichopus japonicus ) . Fish & Shellfish Immunology , 34 ( 1 ): 147 - 158 , https://doi.org/10.1016/j.fsi.2012.10.014 https://doi.org/10.1016/j.fsi.2012.10.014 .

Tang J , Xu L Q , Zeng Y W et al . 2021 . Effect of gut microbiota on LPS-induced acute lung injury by regulating the TLR4/NF-kB signaling pathway . International Immunopharmacology , 91 : 107272 , https://doi.org/10.1016/j.intimp.2020.107272 https://doi.org/10.1016/j.intimp.2020.107272 .

Tibbetts I R . 1997 . The distribution and function of mucous cells and their secretions in the alimentary tract of Arrhamphus sclerolepis krefftii . Journal of Fish Biology , 50 ( 4 ): 809 - 820 , https://doi.org/10.1111/j.1095-8649.1997.tb01974.x https://doi.org/10.1111/j.1095-8649.1997.tb01974.x .

Tran N T , Xiong F , Hao Y T , et al . 2018 . Starvation influences the microbiota assembly and expression of immunity-related genes in the intestine of grass carp ( Ctenopharyngodon idellus ) . Aquaculture , 489 : 121 - 129 , https://doi.org/10.1016/j.aquaculture.2018.02.016 https://doi.org/10.1016/j.aquaculture.2018.02.016 .

Wang L , Zhao X W , Xu H C et al . 2018 . Characterization of the bacterial community in different parts of the gut of sea cucumber ( Apostichopus japonicus ) and its variation during gut regeneration . Aquaculture Research , 49 ( 5 ): 1987 - 1996 , https://doi.org/10.1111/are.13654 https://doi.org/10.1111/are.13654 .

Wang T T , Sun Y X , Jin L J et al . 2013 . Aj -rel and Aj -p105, two evolutionary conserved NF-κB homologues in sea cucumber ( Apostichopus japonicus ) and their involvement in LPS induced immunity . Fish & Shellfish Immunology , 34 ( 1 ): 17 - 22 , https://doi.org/10.1016/j.fsi.2012.09.006 https://doi.org/10.1016/j.fsi.2012.09.006 .

Wang X T , Sun Y X , Wang L L et al . 2017 . Synbiotic dietary supplement affects growth, immune responses and intestinal microbiota of Apostichopus japonicus . Fish & Shellfish Immunology , 68 : 232 - 242 , https://doi.org/10.1016/j.fsi.2017.07.027 https://doi.org/10.1016/j.fsi.2017.07.027 .

Yamazaki Y , Meirelles P M , Mino S et al . 2016 . Individual Apostichopus japonicus fecal microbiome reveals a link with polyhydroxybutyrate producers in host growth gaps . Scientific Reports , 6 : 21631 , https://doi.org/10.1038/srep21631 https://doi.org/10.1038/srep21631 .

Yang G , Xu Z J , Tian X L et al . 2015 . Intestinal microbiota and immune related genes in sea cucumber ( Apostichopus japonicus ) response to dietary β‍-glucan supplementation . Biochemical and Biophysical Research Communications , 458 ( 1 ): 98 - 103 , https://doi.org/10.1016/j.bbrc.2015.01.074 https://doi.org/10.1016/j.bbrc.2015.01.074 .

Yang H S , Yuan X T , Zhou Y et al . 2005 . Effects of body size and water temperature on food consumption and growth in the sea cucumber Apostichopus japonicus (Selenka) with special reference to aestivation . Aquaculture Research , 36 ( 11 ): 1085 - 1092 , https://doi.org/10.1111/j.1365-2109.2005.01325.x https://doi.org/10.1111/j.1365-2109.2005.01325.x .

Yuan X T , Yang H S , Wang L L et al . 2007a . Effects of aestivation on the energy budget of sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea) . Acta Ecologica Sinica , 27 ( 8 ): 3155 - 3161 , https://doi.org/10.1016/S1872-2032(07)60070-5 https://doi.org/10.1016/S1872-2032(07)60070-5 .

Yuan X T , Yang H S , Chen M Y et al . 2007b . Research advances in aestivation of sea cucumber Apostichopus japonicus (Selenka): a review . Marine Sciences , 31 ( 8 ): 88 - 90 , https://doi.‍org/10.3969/j.‍issn.‍1000-3096.2007.08.018. https://doi.‍org/10.3969/j.‍issn.‍1000-3096.2007.08.018. (in Chinese with English abstract)

Zhang H X , Wang Q , Liu S L et al . 2019 . Genomic and metagenomic insights into the microbial community in the regenerating intestine of the sea cucumber Apostichopus japonicus . Frontiers in Microbiology , 10 : 1165 , https://doi.org/10.3389/fmicb.2019.01165 https://doi.org/10.3389/fmicb.2019.01165 .

Zhang H X , Wang Q , Zhao J M et al . 2020 . Quantitative microbiome profiling links microbial community variation to the intestine regeneration rate of the sea cucumber Apostichopus japonicus . Genomics , 112 ( 6 ): 5012 - 5020 , https://doi.org/10.1016/j.ygeno.2020.09.017 https://doi.org/10.1016/j.ygeno.2020.09.017 .

Zhao Y , Liu H , Wang Q et al . 2019a . The effects of benzo [a ] pyrene on the composition of gut microbiota and the gut health of the juvenile sea cucumber Apostichopus japonicus Selenka. Fish & Shellfish Immunology , 93 : 369 - 379 , https://doi.org/10.1016/j.fsi.2019.07.073 https://doi.org/10.1016/j.fsi.2019.07.073 .

Zhao Y , Wang H N , Wang H et al . 2022 . Metabolic response of the sea cucumber Apostichopus japonicus during the estivation-arousal cycles . Frontiers in Marine Science , 9 : 980221 , https://doi.org/10.3389/fmars.2022.980221 https://doi.org/10.3389/fmars.2022.980221 .

Zhao Y , Wang Q , Liu H et al . 2019b . High-throughput sequencing of 16S rRNA amplicons characterizes gut microbiota shift of juvenile sea cucumber Apostichopus japonicus feeding with three antibiotics . Journal of Oceanology and Limnology , 37 ( 5 ): 1714 - 1725 , https://doi.org/10.1007/s00343-019-8308-5 https://doi.org/10.1007/s00343-019-8308-5 .

Zhao Y , Yang H S , Storey K B et al . 2014 . RNA-seq dependent transcriptional analysis unveils gene expression profile in the intestine of sea cucumber Apostichopus japonicus during aestivation . Comparative Biochemistry and Physiology Part D : Genomics and Proteomics , 10 : 30 - 43 , https://doi.org/10.1016/j.cbd.2014.02.002 https://doi.org/10.1016/j.cbd.2014.02.002 .

Zihler F . 1982 . Gross morphology and configuration of digestive tracts of cichlidae (Teleostei, Perciformes): phylogenetic and functional, significance . Netherlands Journal of Zoology , 32 ( 4 ): 544 - 571 , https://doi.org/10.1163/002829682X00210 https://doi.org/10.1163/002829682X00210 .

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