Skip to main content

Advertisement

Springer Nature Link
Log in

Specific patterns and drivers of the bacterial communities in the sediment of two typical integrated multitrophic aquaculture systems

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

The integrated multitrophic aquaculture (IMTA) pond represents a unique ecosystem in which various species of aquatic organisms with different trophic levels are co-cultured together, achieving ecological and economic effects by using ecological principles. This study was designed to investigate the composition pattern of the bacterial communities and potential drivers in IMTA ponds of Penaeus japonicus-Portunus trituberculatus (SC) and P. japonicus-P. trituberculatus-Sinonovacula constricta (SCC). SC and SCC sediments were collected in July, October, and December and used to sequence the 16S rRNA gene and analyze physical and chemical indicators. The α diversity of the bacterial community was not significantly different between the sediments of SC and SCC. The dominant phyla of bacterial communities in sediments of SC and SCC shared a large number of common members. Bacterial members involved in denitrification were biomarkers in the sediment of SC, while biomarkers involved in nitrification, assimilatory nitrate reduction, and nitrogen fixation were found in the sediment of SCC. The β diversity was significantly different between SC and SCC. The bacterial community composition dissimilarity was significantly correlated with environmental factors, which were driven by pH, NH4+ concentration in the sediment (S_ NH4+), and NO2− concentration in the sediment (S_ NO2−) in July, and pH was the most important explanatory variable for the community composition dissimilarity (P < 0.05). The dissimilarity was driven by oxidation–reduction potential (ORP) and NO2− concentration in the pore water of sediments (P_ NO2−) in October, and P_ NO2− was the most important variable (P < 0.05). The S_ NH4+, S_ NO2−, and pH exhibited interactions for the dissimilarity in December, and the S_ NH4+ was the most important variable (P < 0.05). Additionally, the pH was significantly correlated with the S_ NH4+ and S. constricta densities (P < 0.05). These results indicated that the co-culture of S. constricta in shrimp-crab ponds may cause specific composition patterns of bacterial communities by influencing pH and inorganic nitrogen sources, resulting in an increase in bacterial mineralization and nutrient catabolism and a shift in the nitrogen cycling processes from denitrification to nitrification, assimilatory nitrate reduction, and nitrogen fixation in the sediment.

Graphical abstract

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Data availability

Data provided in the paper and supplemental information are available from the corresponding author upon reasonable request.

References

  • Anderson JL, Asche F, Garlock T, Chu J (2017) Aquaculture: its role in the future of food. Front Econ Globalization 17:159–1733

    Article  Google Scholar 

  • Bai LL, Cao CC, Wang CH, Xu HC, Zhang H, Slaveykova VI, Jiang HL (2017) Toward quantitative understanding of the bioavailability of dissolved organic matter in freshwater lake during Cyanobacteria blooming. Crit Rev Env Sci Tec 51:6018–6026

    Article  CAS  Google Scholar 

  • Brackin R, Robinson N, Lakshmanan P, Schmidt S (2013) Microbial function in adjacent subtropical forest and agricultural soil. Soil Biol Biochem 57:68–77

    Article  CAS  Google Scholar 

  • Buck BH, Troell MF, Krause G, Angel DL, Grote B, Chopin T (2018) State of the art and challenges for offshore integrated multi-trophic aquaculture (IMTA). Front Mar Sci 5:1–21

    Article  Google Scholar 

  • Chang ZQ, Neori A, He YY, Li JT, Preston QL, SI, Liu P, Li J, (2020) Development and current state of seawater shrimp farming, with an emphasis on integrated multi-trophic pond aquaculture farms, in China- a review. Rev Aquacult 12:2544–2558

    Article  Google Scholar 

  • Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Evol S 31:343–366

    Article  Google Scholar 

  • Dyksma S, Lenk S, Sawicka JE, Mußmann M (2018) Uncultured Gammaproteobacteria and Desulfobacteraceae account for major acetate assimilation in a coastal marine sediment. Front Microbiol 9:1–10

    Article  Google Scholar 

  • Edgar RC (2013) UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Edwards JS, Battista JR (2003) Using DNA microarray data to understand the ionizing radiation resistance of Deinococcus radiodurans. Trends Biotechnol 21:381–382

    Article  CAS  PubMed  Google Scholar 

  • Erb M (2018) Volatiles as inducers and suppressors of plant defense and immunity- origins, specificity, perception and signaling. Curr Opin Plant Biol 44:117–121

    Article  CAS  PubMed  Google Scholar 

  • Ettoumi B, Guesmi A, Brusetti L, Borin S, Najjari A, Boudabous A, Cherif A (2013) Microdiversity of deep-sea Bacillales isolated from Tyrrhenian sea sediments as revealed by ARISA, 16S rRNA gene sequencing and BOX-PCR fingerprinting. Microbes Environ 28:361–369

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan LM, Barry K, Hu GD, Meng SL, Song C, Qiu LP, Zheng Y, Wu W, Qu JH, Chen JZ, Xu P (2017) Characterizing bacterial communities in tilapia pond surface sediment and their responses to pond differences and temporal variations. World J Microb Biot 33:1

    Article  CAS  Google Scholar 

  • Feng BW, Li XR, Wang JH, Hu ZY, Meng H, Xiang LY, Quan ZX (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. Fems Microbiol Eco 70:236–248

    Article  CAS  Google Scholar 

  • Flores E, Arévalo S, Burnat M (2019) Cyanophycin and arginine metabolism in cyanobacteria. Algal Res 42:101577

    Article  Google Scholar 

  • Gonzalez SV, Johnston E, Gribben PE, Dafforn K (2019) The application of bioturbators for aquatic bioremediation: review and meta-analysis. Environ Pollut 250:426–436

    Article  CAS  Google Scholar 

  • Herrero A, Flores E (2019) Genetic responses to carbon and nitrogen availability in Anabaena. Environ Microbiol 21:1–17

    Article  CAS  PubMed  Google Scholar 

  • Hollister EB, Engledow AS, Hammett AJM, Provin TL, Wilkinson HH, Gentry TJ (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:829–838

    Article  CAS  PubMed  Google Scholar 

  • Hoshino T, Doi H, Uramoto GI, Wormer L, Adhikari RR, Xiao N, Morono Y, D’Hondt S, Hinrichs KU, Inagaki F (2020) Global diversity of microbial communities in marine sediment. P Natl Acad Sci USA 117:27587–27597

    Article  CAS  Google Scholar 

  • Hu WC, Liang JS, Ju F, Wang QJ, Liu RP, Bai YH, Liu HJ, Qu JH (2020) Metagenomics unravels differential microbiome composition and metabolic potential in rapid sand filters purifying surface water versus groundwater. Environ Sci Technol 54:5197–5206

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Pan LQ, Song MS, Tian CC, Gao S (2018) Microbiota assemblages of water, sediment, and intestine and their associations with environmental factors and shrimp physiological health. Appl Microbiol Biot 102:8585–8598

    Article  CAS  Google Scholar 

  • Jansson JK, Taş N (2014) The microbial ecology of permafrost. Nat Rev Microbiol 12:414–425

    Article  CAS  PubMed  Google Scholar 

  • Jiang W, Tian X, Li L, Jiang WW, Tian XL, Li L, Dong SL, Zhao K, Li HD, Cai YY (2019) Temporal bacterial community succession during the start-up process of biofilters in a cold-freshwater recirculating aquaculture system. Bioresource Technol 287:121441

    Article  CAS  Google Scholar 

  • Jiao S, Yang YF, Xu YQ, Zhang J, Lu YH (2020) Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. ISME J 14:202–216

    Article  PubMed  Google Scholar 

  • Jones CM, Graf DRH, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426

    Article  CAS  PubMed  Google Scholar 

  • Kong HG, Song GC, Sim HJ, Ryu CM (2021) Achieving similar root microbiota composition in neighbouring plants through airborne signalling. ISME J 15:397–408

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Ng DHP, Wu YC, Cao B (2019) Microbial community composition and putative biogeochemical functions in the sediment and water of Tropical Granite Quarry Lakes. Microb Ecol 77:1–11

    Article  CAS  PubMed  Google Scholar 

  • Laffite A, Florio A, Andrianarisoa KS, Des Chatelliers CC, Schloter-Hai B, Ndaw SM, Periot C, Schloter M, Zeller B, Poly F, Le Roux X (2020) Biological inhibition of soil nitrification by forest tree species affects Nitrobacter populations. Environ Microbio 22:1141–1153

    Article  CAS  Google Scholar 

  • Laskov C, Herzog C, Lewandowski J, Hupfer M (2007) Miniaturized photometrical methods for the rapid analysis of phosphate, ammonium, ferrous iron, and sulfate in pore water of freshwater sediments. Limnol Oceanogr-Meth 5:63–71

    Article  CAS  Google Scholar 

  • Liang YT, Zhang YY, Zhou C, Li HM, Kang XM, Wang L, Song JM, Jiao NZ (2019) Cumulative impact of long-term intensive mariculture on total and active bacterial communities in the core sediments of the Ailian Bay, North China. Sci Total Environ 691:1212–1224

    Article  CAS  PubMed  Google Scholar 

  • Lin J, Ju B, Yao YN, Lin XM, Xing RL, Teng L, Jiang AL (2016) Microbial community in a multi-trophic aquaculture system of Apostichopus japonicus, Styela clava and microalgae. Aquacult Int 24:1119–1140

    Article  CAS  Google Scholar 

  • Lu SD, Sun YJ, Lu BY, Zheng DY, Xu SW (2020) Change of abundance and correlation of Nitrospira inopinata-like comammox and populations in nitrogen cycle during different seasons. Chemosphere 241:125098

    Article  CAS  PubMed  Google Scholar 

  • Lukwambe B, Nicholaus R, Zhao L, Yang W, Zhu J, Zheng Z (2020) Microbial community and interspecies interaction during grazing of ark shell bivalve (Scapharcasubcrenata) in a full-scale bioremediation system of mariculture effluents. Mar Environ Res 158:104956

    Article  CAS  PubMed  Google Scholar 

  • Lukwambe B, Yang W, Zheng YQ, Nicholaus R, Zhu JY, Zheng ZM (2018) Bioturbation by the razor clam (Sinonovacula constricta) on the microbial community and enzymatic activities in the sediment of an ecological aquaculture wastewater treatment system. Sci Total Environ 643:1098–1107

    Article  CAS  PubMed  Google Scholar 

  • Luo YQ, Feng LJ, Jia R, Yang GF, Yang Q, Mu J (2020) Variation in microbial populations and antibiotic resistance genes in mariculture sediments in the present of the seaweed Ulva fasciata and under selective pressure of oxytetracycline. Ecotox Environ Safe 204:111114

    Article  CAS  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  PubMed  PubMed Central  Google Scholar 

  • Na H, Lever MA, Kjeldsen KU, Schulz F, Jørgensen BB (2015) Uncultured Desulfobacteraceae and Crenarchaeotal group C3 incorporate 13C-acetate in coastal marine sediment. Env Microbiol Rep 7:614–622

    Article  CAS  Google Scholar 

  • Obiero K, Meulenbroek P, Drexler S, Dagne A, Akoll P, Odong R, Kaunda-Arara B, Waidbacher H (2019) The contribution of fish to food and nutrition security in Eastern Africa: Emerging trends and future outlooks. Sustainability-BASEL 11:1–15

    Google Scholar 

  • Omont A, Elizondo-González R, Quiroz-Guzmán E, Escobedo-Fregoso C, Hernández-Herrera R, Peña-Rodríguez A (2020) Digestive microbiota of shrimp Penaeusvannamei and oyster Crassostreagigas co-cultured in integrated multi-trophic aquaculture system. Aquaculture 521:735059

    Article  CAS  Google Scholar 

  • Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL (2010) Highly specialized microbial diversity in hyper-arid polar desert. P Natl Acad Sci USA 107:1254–1254

    Article  CAS  Google Scholar 

  • Samocha TM, Fricker J, Ali AM, Shpigel M, Neori A (2015) Growth and nutrient uptake of the macroalga Gracilaria tikvahiae cultured with the shrimp Litopenaeus vannamei in an integrated multi-trophic aquaculture (IMTA) system. Aquaculture 446:263–271

    Article  Google Scholar 

  • Sanz-Lazaro C, Sanchez-Jerez P (2020) Regional integrated multi-trophic aquaculture (RIMTA): spatially separated, ecologically linked. J Environ Manage 271:110921

    Article  PubMed  Google Scholar 

  • Scarlett K, Denman S, Clark DR, Vanguelova E, Brown N, Whitby C (2020) Relationships between nitrogen cycling microbial community abundance and composition reveal the indirect effect of soil pH on oak decline. ISME J 15:623–635

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, Li XY, Liang WJ, Chu HY (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211

    Article  CAS  Google Scholar 

  • Stackebrandt E, Goebel BM (1994) A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Micr 44:846–849

    Article  CAS  Google Scholar 

  • Stivaletta N, Ĺopez-Garćia P, Boihem L, Millie DF, Barbieri R (2010) Biomarkers of endolithic communities within gypsum crusts (Southern Tunisia). Geomicrobiol J 27:101–110

    Article  CAS  Google Scholar 

  • Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, Djahanschiri B, Zeller G, Mende DR, Alberti A, Cornejo-Castillo FM, Costea PI, Cruaud C, d’Ovidio F, Engelen S, Ferrera I, Gasol JM, Guidi L, Hildebrand F, Kokoszka F, Lepoivre C, Lima-Mendez G, Poulain J, Poulos BT, Royo-Llonch M, Sarmento H, Vieira-Silva S, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Bowler C, de Vargas C, Gorsky G, Grimsley N, Hingamp P, Iudicone D, Jaillon O, Not F, Ogata H, Pesant S, Speich S, Stemmann L, Sullivan MB, Weissenbach J, Wincker P, Karsenti E, Raes J, Acinas SG, Bork P, Tara Oceans C (2015) Structure and function of the global ocean microbiome. Science 348:1–10

    Article  Google Scholar 

  • Tu XH, Xiao BD, Xiong JA, Chen XD (2010) A simple miniaturised photometrical method for rapid determination of nitrate and nitrite in freshwater. Talanta 82:976–983

    Article  CAS  PubMed  Google Scholar 

  • Wang XB, Lü XT, Yao J, Wang ZW, Deng Y, Cheng WX, Zhou JZ, Han XG (2017) Habitat-specific patterns and drivers of bacterial β-diversity in China’s drylands. ISME J 11:1345–1358

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73:5261–5267

    Article  CAS  Google Scholar 

  • Xu CY, Lv ZQ, Shen YB, Liu DJ, Fu YL, Zhou L, Liu W, Chen K, Ye HL, Xia X, Xia JJ, Wang Y, Ke YB, Shen JZ (2020) Metagenomic insights into differences in environmental resistome profiles between integrated and monoculture aquaculture farms in China. Environ Int 144:106005

    Article  PubMed  Google Scholar 

  • Yan LJ, Herrmann M, Kampe B, Lehmann R, Totsche KU, Küsel K (2020) Environmental selection shapes the formation of near-surface groundwater microbiomes. Water Res 170:115341

    Article  CAS  PubMed  Google Scholar 

  • Yao L, Chen C, Liu G, Li F, Liu W (2018) Environmental factors, but not abundance and diversity of nitrifying microorganisms, explain sediment nitrification rates in Yangtze Lakes. RSC Adv 8:1875–1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang DX, Tian XL, Dong SL, Chen Y, Feng J, He RP, Zhang K (2019a) Methane fluxes from typical marine polyculture ponds of swimming crab with kuruma shrimp and short-necked clam in eastern China. Aquacult Env Interac 11:63–73

    Article  CAS  Google Scholar 

  • Zhang MY, Pan LQ, Huang F, Gao S, Su C, Zhang MZ, He ZY (2019b) Metagenomic analysis of composition, function and cycling processes of microbial community in water, sediment and effluent of Litopenaeus vannamei farming environments under different culture modes. Aquaculture 506:280–293

    Article  Google Scholar 

  • Zhang XM, Johnston ER, Li LH, Konstantinidis KT, Han XG (2017) Experimental warming reveals positive feedbacks to climate change in the Eurasian Steppe. ISME J 11:885–895

    Article  CAS  PubMed  Google Scholar 

  • Zhao DY, Shen F, Zeng J, Huang R, Yu ZB, Wu QLL (2016) Network analysis reveals seasonal variation of co-occurrence correlations between Cyanobacteria and other bacterioplankton. Sci Total Environ 573:817–825

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. Fang Wang (Ocean University of China) for her guidance and advices on the experimental design. The authors also thank Changjian Li, Yizhuo, Jiang, Wenheng Li, Liye Yu, and Weijia Pu for their assistance during sample collection.

Funding

This work is supported by the National Key R&D Program of China, no.2019YFD0900402.

Author information

Authors and Affiliations

  1. The Key Laboratory of Mariculture (Ocean University of China), Ministry of Education, Qingdao, 266003, China

    Qian Liu, Junnan Li, Hongwei Shan & Yicheng Xie

  2. Zhejiang Marine Fisheries Research Institute, Zhoushan, 316021, China

    Dongxu Zhang

Authors
  1. Qian Liu
    View author publications

    Search author on:PubMed Google Scholar

  2. Junnan Li
    View author publications

    Search author on:PubMed Google Scholar

  3. Hongwei Shan
    View author publications

    Search author on:PubMed Google Scholar

  4. Yicheng Xie
    View author publications

    Search author on:PubMed Google Scholar

  5. Dongxu Zhang
    View author publications

    Search author on:PubMed Google Scholar

Contributions

Liu Qian: sample collection, sample determination, writing—original draft; Li Junnan: data curation, writing—original draft, formal analysis; Shan Hongwei: methodology, writing—review and editing, supervision; Xie Yicheng: sample collection, sample determination; Zhang Dongxu: data curation.

Corresponding author

Correspondence to Hongwei Shan.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Mauricio Gustavo Coelho Emerenciano

Publisher's note

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

Highlights

• Specific patterns and the drivers of the bacterial community in the sediment of two typical IMTA systems (shrimp-crab ponds and shrimp-crab-clam ponds) were studied.

• The α diversity of the bacterial community was not significantly different, whereas the β diversity was significantly different in shrimp-crab ponds and shrimp-crab-clam ponds.

• Clams caused differences in the bacterial community by influencing the physical and chemical factors of the sediment, and pH and NH4+ concentration were the dominant factors.

• The effects of clams on pH and inorganic nitrogen sources potentially shifted the nitrogen cycling process from denitrification to nitrification, assimilatory nitrate reduction and nitrogen fixation.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 36.8 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Q., Li, J., Shan, H. et al. Specific patterns and drivers of the bacterial communities in the sediment of two typical integrated multitrophic aquaculture systems. Aquacult Int 30, 1369–1388 (2022). https://doi.org/10.1007/s10499-022-00862-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-022-00862-2

Keywords

Profiles

  1. Hongwei Shan View author profile