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Evaluation of the Physiological Bacterial Groups in a Tropical Biosecured, Zero-Exchange System Growing Whiteleg Shrimp, Litopenaeus vannamei

  • Environmental Microbiology
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Abstract

To elucidate the individual and multiple roles of physiological bacterial groups involved in biogeochemical cycles of carbon, nitrogen, phosphorus and sulfur, the changes in the abundance of aerobic bacteria (heterotrophs, methane oxidizers, ammonia oxidizers, sulfur oxidizers, phosphate solubilizers, phosphate accumulators) and anaerobic bacteria (total anaerobes, nitrate reducers, denitrifiers and sulfate reducers) were investigated in a biosecured, zero-exchange system stocked with whiteleg shrimp, Litopenaeus vannamei for one production cycle. Key water quality parameters during the 96-day production cycle fell within the normal range for L. vannamei culture. Results of Spearman’s correlation matrix revealed that different sets of variables correlated at varying levels of significance of the interrelationships between bacterial abundances and water quality parameters. The three nitrogenous species (ammonia, nitrite and nitrate) strongly influenced the physiological bacterial groups’ abundance. The strong relationship of bacterial groups with phytoplankton biomass and abundance clearly showed the trophic interconnections in nutrient exchange/recycling. Canonical correspondence analysis performed to assess the total variation revealed that the three dissolved nitrogen species followed by salinity, temperature, phytoplankton biomass and pH collectively accounted for as much as 82% of the total variation. In conclusion, the results of the study revealed that the major drivers that interweaved biogeochemical cycles are the three dissolved nitrogen species, which microbially mediated various aerobic-anaerobic assimilation/dissimilation processes in the pond ecosystem. Considering the pond microbial ecology becoming an important management tool where applied research could improve the economic and environmental sustainability of the aquaculture industry, the findings of the present study are practically relevant.

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References

  1. Yuan J, Jian X, Deyan L, Hojeong K, Tiehu He Sunghyun K, Yongxin L, Chris F, Weixin D (2019) Rapid growth of greenhouse gas emissions from the adoption of industrial-scale aquaculture. Nat Clim Chang 9(4):318–322. https://doi.org/10.1038/s41558-019-0425-9

    Article  Google Scholar 

  2. FAO (2020) The state of world fisheries and aquaculture 2020 Sustainability in action. Rome. https://doi.org/10.4060/ca9229en

  3. Fernandes V, Sabu EA, Shivaramu MS, Gonsalves MJB, Sreepada RA (2019) Dynamics and succession of plankton communities with changing nutrient levels in tropical culture ponds of whiteleg shrimp. Aquacult Env Interac 11:639–655. https://doi.org/10.3354/aei00341

    Article  Google Scholar 

  4. Alfiansah YR, Hassenrück C, Kunzmann A, Taslihan A, Harder J, Gärdes A (2018) Bacterial abundance and community composition in pond water from shrimp aquaculture systems with different stocking densities. Front Microbiol 9:2457. https://doi.org/10.3389/fmicb.2018.02457

    Article  PubMed  PubMed Central  Google Scholar 

  5. Ray AJ, Dillon KS, Lotz JM (2011) Water quality dynamics and shrimp (Litopenaeus vannamei) production in intensive, mesohaline culture systems with two levels of biofloc management. Aquac Eng 45:127–136. https://doi.org/10.1016/j.aquaeng.2011.09.001

    Article  Google Scholar 

  6. Ray AJ, Seaborn G, Leffler JW, Wilde SB, Lawson A, Browdy CL (2010) Characterization of microbial communities in minimal-exchange, intensive aquaculture systems and the effects of suspended solids management. Aquaculture 310:130–138. https://doi.org/10.1016/j.aquaculture.2010.10.019

    Article  Google Scholar 

  7. Schock TB, Duke J, Goodson A, Weldon D, Brunson J, Leffler JW, Bearden DW (2013) Evaluation of Pacific white shrimp (Litopenaeus vannamei) health during a superintensive aquaculture growout using NMR-based metabolomics. PLoS One 8:e59521. https://doi.org/10.1371/journal.pone.0059521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Briggs MRP, Funge-Smith SJ (1994) A nutrient budget of some intensive marine shrimp ponds in Thailand. Aquac Res 25(8):789–811. https://doi.org/10.1111/j.1365-2109.1994.tb00744.x

    Article  Google Scholar 

  9. Funge-Smith SJ, Briggs MR (1998) Nutrient budgets in intensive shrimp ponds: implications for sustainability. Aquaculture 164:117–133. https://doi.org/10.1016/S0044-8486(98)00181

    Article  Google Scholar 

  10. Richard G, Boiffin J, Duval Y (1995) Direct drilling of sugar beet into cover crop: effects on soil physical conditions and crop establishment. Soil Till Res 34:169–185. https://doi.org/10.1016/0167-1987(95)00464-4

    Article  Google Scholar 

  11. Mishra JK, Samocha TM, Patnaik S, Speed M, Gandy RL, Ali AM (2008) Performance of an intensive nursery system for the Pacific white shrimp, Litopenaeus vannamei, under limited discharge condition. Aquac Eng 38:2–15. https://doi.org/10.1016/j.aquaeng.2007.10.003

    Article  Google Scholar 

  12. Lananan F, Hamid SHA, Din WNS, Khatoon H, Jusoh A, Endut A (2014) Symbiotic bioremediation of aquaculture wastewater in reducing ammonia and phosphorus utilizing effective microorganism (EM-1) and microalgae (Chlorella sp.). Int Biodeterior Biodegradation 95:127–134. https://doi.org/10.1016/j.ibiod.2014.06.013

    Article  CAS  Google Scholar 

  13. Focht DD, Verstraete W (1977) Biochemical ecology of nitrification and denitrification. Adv Microb Ecol Plenum N Y 1:135–214. https://doi.org/10.1007/978-1-4615-8219-9_4

    Article  CAS  Google Scholar 

  14. Sahu MK, Swarnakumar NS, Sivakumar K, Thangaradjou T, Kannan L (2008) Probiotics in aquaculture: importance and future perspectives. Indian J Microbiol 48:299–308. https://doi.org/10.1007/s12088-008-0024-3

    Article  PubMed  PubMed Central  Google Scholar 

  15. Van Rijn J, Tal Y, Schreier HJ (2006) Denitrification in recirculating systems: theory and applications. Aquac Eng 34:364–376. https://doi.org/10.1016/j.aquaeng.2005.04.004

    Article  Google Scholar 

  16. Queiroz HM, Adriana GA, Carlos AK, Taniguchi MRSS, Juliana CN, Gabriel NN, Xosé LO, Tiago OF (2019) Hidden contribution of shrimp farming effluents to greenhouse gas emissions from mangrove soils. Estuar Coast Shelf Sci 221:8–14. https://doi.org/10.1016/j.ecss.2019.03.011

    Article  CAS  Google Scholar 

  17. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for sea water analysis. Pergamon Press, Oxford, pp 63–104. https://doi.org/10.1016/C2009-0-07774-5

  18. Rodina AG (1972) In: Colwell RR, Zambruski MS (eds) Methods in aquatic microbiology. University Park Press, Baltimore. https://doi.org/10.1002/jobm.19730130834

    Chapter  Google Scholar 

  19. LokaBharathi PA, Chandramohan D (1990) Sulfate-reducing bacteria from the Arabian Sea—their distribution in relation to thiosulfate-oxidizing and heterotrophic bacteria. Bull Mar Sci 47:622–630

    Google Scholar 

  20. Whittenbury R, Phillips KC, Wilkinson JF (1970) Enrichment, isolation and some properties of methane utilizing bacteria. Microbiology 61:205–218. https://doi.org/10.1099/00221287-61-2-205

    Article  CAS  Google Scholar 

  21. Jørgensen KS, Pauli ASL (1995) Polyphosphate accumulation among denitrifying bacteria in activated sludge. Anaerobe 1:161–168. https://doi.org/10.1006/anae.1995.1014

    Article  PubMed  Google Scholar 

  22. Hoppe HG (1988) Methods in aquatic bacteriology.(modern microbiological methods), Austin B (Ed.), vol XXI. Wiley, Chichester, p 425

    Google Scholar 

  23. Ram A, LokaBharathi PA, Nair S, Chandramohan D (2001) A deep-sea bacterium with unique nitrifying property. Curr Sci India 80:1222–1224. http://drs.nio.org/drs/handle/2264/266. Accessed 17 Aug 2020

  24. Bonin P (1996) Anaerobic nitrate reduction to ammonium in two strains isolated from coastal marine sediment: a dissimilatory pathway. FEMS Microbiol Ecol 19:27–38. https://doi.org/10.1111/j.1574-6941.1996.tb00195.x

    Article  CAS  Google Scholar 

  25. Zar JH (1996) Biostatistical analysis. Prentice Hall, Upper Saddle River, p 481

    Google Scholar 

  26. ter Braak CJF, Šmilauer P (2002) CANOCO Reference manual and CanoDraw for Windows user’s guide — software for canonical community ordination, version 4.5. Microcomputer Power, Publisher Biometris, Ithaca, pp 500

  27. ter Braak CJ, Verdonschot PF (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57:255–289. https://doi.org/10.1007/BF00877430

    Article  Google Scholar 

  28. Chien YH (1992) Water quality requirements and management for marine shrimp culture. In: Wyban J (ed) Proceedings of the Special Session on Shrimp Farming. World Aquaculture Society, Baton Rouge, pp 30–42

    Google Scholar 

  29. Bai Y, Qi W, Liang J, Qu J (2014) Using high-throughput sequencing to assess the impacts of treated and untreated wastewater discharge on prokaryotic communities in an urban river. Appl Microbiol Biotechnol 98:1841–1851. https://doi.org/10.1007/s00253-013-5116-2

    Article  CAS  PubMed  Google Scholar 

  30. Zoqratt MZHM, Eng WWH, Thai BT, Austin CM, Gan HM (2018) Microbiome analysis of Pacific white shrimp gut and rearing water from Malaysia and Vietnam: implications for aquaculture research and management. Peer J 6:e5826. https://doi.org/10.7717/peerj.5826

  31. Fernandes SO, Kulkarni SS, Shirodkar RR, Karekar SV, Kumar RP, Sreepada RA, LokaBharathi PA (2010) Water quality and bacteriology in an aquaculture facility equipped with a new aeration system. Environ Monit Assess 64:81–92. https://doi.org/10.1007/s10661-009-0876-y

    Article  CAS  Google Scholar 

  32. Burford MA, Williams KC (2001) The fate of nitrogenous waste from shrimp feeding. Aquaculture 198:79–93. https://doi.org/10.1016/S0044-8486(00)00589-5

    Article  CAS  Google Scholar 

  33. Burford MA, Costanzo SD, Dennison WC, Jackson CJ, Jones AB, McKinnon AD, Preston NP, Trott LA (2003) A synthesis of dominant ecological processes in intensive shrimp ponds and adjacent environments in NE Australia. Mar Pollut Bull 46:1456–1469. https://doi.org/10.1016/S0025-326X(03)00282-0

    Article  CAS  PubMed  Google Scholar 

  34. Alongi DM, Johnston DJ, Xuan TT (2000) Carbon and nitrogen budgets in shrimp ponds of extensive mixed shrimp–mangrove forestry farms in the Mekong Delta, Vietnam. Aquac Res 31:387–399. https://doi.org/10.1046/j.1365-2109.2000.00457.x

    Article  Google Scholar 

  35. Shariff M, Yusoff FM, Devaraja TN, Rao PS (2001) The effectiveness of a commercial microbial product in poorly prepared tiger shrimp, Penaeus monodon (Fabricius), ponds. Aquac Res 32:181–187. https://doi.org/10.1046/j.1365-2109.2001.00543.x

    Article  CAS  Google Scholar 

  36. Abraham TJ, Ghosh S, Nagesh S, Sasmal D (2004) Distribution of bacteria involved in nitrogen and sulphur cycles in shrimp culture systems of West Bengal, India. Aquaculture 239:275–288. https://doi.org/10.1016/j.aquaculture.2004.06.023

    Article  CAS  Google Scholar 

  37. Krishnani KK, Kathiravan V (2010) A quantitative method for detecting ammoniaoxidizing bacteria in coastal aquaculture systems. Aquac Res 41:1648–1657. https://doi.org/10.1111/j.1365-2109.2010.02535.x

    Article  CAS  Google Scholar 

  38. Castine SA, Erler DV, Trott LA, Paul NA, De Nys R, Eyre BD (2012) Denitrification and anammox in tropical aquaculture settlement ponds: an isotope tracer approach for evaluating N2 production. PloS One 7:e42810. https://doi.org/10.1371/journal.pone.0042810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kathiravan V, Krishnani KK (2014) Diversity of denitrifying bacteria in the greenwater system of coastal aquaculture. Int Aqua Res 6:135–145. https://doi.org/10.1007/s40071-014-0074-6

    Article  Google Scholar 

  40. Gao D, Liu M, Hou L, Derrick YL, Wang W, Li X, Zeng A, Zheng Y, Han P, Yang Y, Yin G (2019) Effects of shrimp-aquaculture reclamation on sediment nitrate dissimilatory reduction processes in a coastal wetland of southeastern China. Environ Pollut 255:113219. https://doi.org/10.1016/j.envpol.2019.113219

    Article  CAS  PubMed  Google Scholar 

  41. Rao PSS, Karunasagar I, Otta SK, Karunasagar I (2000) Incidence of bacteria involved in nitrogen and sulphur cycles in tropical shrimp culture ponds. Aquacult Int 8:463–472

    Article  CAS  Google Scholar 

  42. Devaraja TN, Yusoff M, Shariff M (2002) Changes in bacterial populations and shrimp production in ponds treated with commercial microbial products. Aquaculture 206:245–256. https://doi.org/10.1016/S0044-8486(01)00721-9

    Article  Google Scholar 

  43. Krishnani KK, Kathiravan V, Natarajan M, Kailasam M, Pillai SM (2010) Diversity of sulfur-oxidizing bacteria in greenwater system of coastal aquaculture. Appl Biochem Biotech 162:1225–1237. https://doi.org/10.1007/s12010-009-8886-3

    Article  CAS  Google Scholar 

  44. Patil PK, Muralidhar M, Solanki HG, Patel PP, Patel K, Gopal C (2016) Effect of culture intensity and probiotics application on microbiological and environmental parameters in Litopenaeus vannamei culture ponds. J Environ Biol 37:21–29

    CAS  PubMed  Google Scholar 

  45. Ghosh M, Chattopadhyay NR (2005) Effects of carbon/nitrogen/phosphorus ratio on mineralizing bacterial population in aquaculture systems. J Appl Aquac 17:85–98. https://doi.org/10.1300/J028v17n02_07

    Article  Google Scholar 

  46. Tendencia EA, Bosma RH, Primavera JH, Vereth JA (2012) Effect of different mangrove-to-pond area ratios on influent water quality and WSSV occurrence in Penaeus monodon semi-intensive farms using the greenwater culture technique. Aquaculture 362–363:72–79. https://doi.org/10.1016/j.aquaculture.2012.07.020

    Article  Google Scholar 

  47. Tendencia EA, Bosma RH, Verdegem MC, Verreth JA (2015) The potential effect of greenwater technology on water quality in the pond culture of Penaeus monodon Fabricius. Aquac Res 46(1):1–13. https://doi.org/10.1111/are.12152

    Article  CAS  Google Scholar 

  48. Jana BB, Chakraborty P, Biswas JK, Ganguly S (2001) Biogeochemical cycling bacteria as indices of pond fertilization: importance of CNP ratios of input fertilizers. J Appl Microbiol 90:733–740. https://doi.org/10.1046/j.1365-2672.2001.01299.x

    Article  CAS  PubMed  Google Scholar 

  49. Ebeling JM, Timmons MB, Bisogni JJ (2006) Engineering analysis of the stoichiometry of photoautotrophic, autotrophic, and heterotrophic removal of ammonia–nitrogen in aquaculture systems. Aquaculture 257:346–358. https://doi.org/10.1016/j.aquaculture.2006.03.019

    Article  Google Scholar 

  50. Lemmonier H, Courties C, Mugnier C, Torreton JP, Herbland A (2010) Nutrient and microbial dynamics in eutrophying shrimp ponds affected or unaffected by vibriosis. Mar Pollut Bull 60:402–411. https://doi.org/10.1016/j.marpolbul.2009.10.012

    Article  CAS  Google Scholar 

  51. Tsukuda S, Christianson L, Kolb A, Saito K, Summerfelt S (2015) Heterotrophic denitrification of aquaculture effluent using fluidized sand biofilters. Aquac Eng 64:49–59. https://doi.org/10.1016/j.aquaeng.2014.10.010

    Article  Google Scholar 

  52. Løvdal T, Eichner C, Grossart HP, Carbonnel V, Chou L, Martin-Jezequel V, Thingstad TF (2008) Competition for inorganic and organic forms of nitrogen and phosphorous between phytoplankton and bacteria during an Emiliania huxleyi spring bloom. Biogeosciences 5:371–383. https://doi.org/10.5194/bg-5-371-2008

  53. Zeng RJ, Lemaire R, Yuan Z, Keller J (2003) Simultaneous nitrification, denitrification, and phosphorus removal in a lab–scale sequencing batch reactor. Biotechnol Bioeng 84:170–178. https://doi.org/10.1002/bit.10744

    Article  CAS  PubMed  Google Scholar 

  54. Barak Y, Van Rijn J (2000) Relationship between nitrite reduction and active phosphate uptake in the phosphate-accumulating denitrifier Pseudomonas sp. Strain JR 12. Appl Environ Microbiol 66:5236–5240. https://doi.org/10.1128/AEM.66.12.5236-5240.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Figdore BA, Stensel HD, Winkler MKH (2018) Bioaugmentation of sidestream nitrifying-denitrifying phosphorus-accumulating granules in a low-SRT activated sludge system at low temperature. Water Res 135:241–250. https://doi.org/10.1016/j.watres.2018.02.035

    Article  CAS  PubMed  Google Scholar 

  56. Zheng L, Ren M, Xie E, Ding A, Liu Y, Deng S, Zhang D (2019) Roles of phosphorus sources in microbial community assembly for the removal of organic matters and ammonia in activated sludge. Front Microbiol 10:1023. https://doi.org/10.3389/fmicb.2019.01023

    Article  PubMed  PubMed Central  Google Scholar 

  57. Foesel BU, Gieseke A, Schwermer C, Stief P, Koch L, Cytryn E, De La Torré JR, Van Rijn J, Minz D, Drake HL, Schramm A (2008) Nitrosomonas Nm143-like ammonia oxidizers and Nitrospira marina-like nitrite oxidizers dominate the nitrifier community in a marine aquaculture biofilm. FEMS Microbiol Ecol 63:192–104. https://doi.org/10.1111/j.1574-6941.2007.00418.x

    Article  CAS  PubMed  Google Scholar 

  58. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996. https://doi.org/10.1104/pp.111.175448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Jackson C, Preston N, Thompson PJ, Burford M (2003) Nitrogen budget and effluent nitrogen components at an intensive shrimp farm. Aquaculture 218:397–411. https://doi.org/10.1016/S0044-8486(03)00014-0

    Article  CAS  Google Scholar 

  60. Brune DE, Kirk K, Eversole AG (2004) Autotrophic intensification of pond aquaculture; shrimp production in a partitioned aquaculture system. Proceedings of the Fifth International Conference on Recirculating Aquaculture, Roanoke, pp 201–210

    Google Scholar 

  61. Casillas-Hernández R, Nolasco-Soria H, García-Galano T, Carrillo-Farnes O, Páez-Osuna F (2007) Water quality, chemical fluxes and production in semi-intensive Pacific white shrimp (Litopenaeus vannamei) culture ponds utilizing two different feeding strategies. Aquac Eng 36:105–114. https://doi.org/10.1016/j.aquaeng.2006.09.001

    Article  Google Scholar 

  62. Hargreaves JA (1998) Nitrogen biogeochemistry of aquaculture ponds. Aquaculture 166:181–212. https://doi.org/10.1016/S0044-8486(98)00298-1

    Article  CAS  Google Scholar 

  63. Hargreaves JA, Tucker CS (2004) Managing ammonia in fish ponds, vol 4603. Southern Regional Aquaculture Center, Stoneville

    Google Scholar 

  64. Metcalf Eddy I (2003) Wastewater Engineering Treatment and Reuse4th edn. McGraw-Hill, New York

    Google Scholar 

  65. Van Rijn J (1996) The potential for integrated biological treatment systems in recirculating fish culture–a review. Aquaculture 139:181–201. https://doi.org/10.1016/0044-8486(95)01151-X

    Article  Google Scholar 

  66. Shapleigh JP (2009) Dissimilatory and assimilatory nitrate reduction in the purple photosynthetic bacteria. The purple phototrophic bacteria. Springer, Dordrecht, pp 623–642

    Chapter  Google Scholar 

  67. Jones ZL, Jasper JT, Sedlak DL, Sharp JO (2017) Sulfide-induced dissimilatory nitrate reduction to ammonium supports anaerobic ammonium oxidation (anammox) in an open-water unit process wetland. Appl Environ Microbiol 83:e00782–e00717. https://doi.org/10.1128/AEM.00782-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Yang P, Zhang Y, Lai DY, Tan L, Jin B, Tong C (2018) Fluxes of carbon dioxide and methane across the water-atmosphere interface of aquaculture shrimp ponds in two subtropical estuaries: the effect of temperature, substrate, salinity and nitrate. Sci Total Environ 635:1025–1035. https://doi.org/10.1016/j.scitotenv.2018.04.102

    Article  CAS  PubMed  Google Scholar 

  69. Trotsenko YA, Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 63:183–229. https://doi.org/10.1016/S0065-2164(07)00005-6

    Article  CAS  PubMed  Google Scholar 

  70. Stein LY, Klotz MG (2011) Nitrifying and denitrifying pathways of methanotrophic bacteria. Biochem Soc Trans 39:1826–1831. https://doi.org/10.1042/BST20110712

    Article  CAS  PubMed  Google Scholar 

  71. Yang P, Lai DYF, Huang JF, Tong C (2018) Effect of drainage on CO2, CH4, and N2O fluxes from aquaculture ponds during winter in a subtropical estuary of China. J Environ Sci (China) 65:72–82. https://doi.org/10.1016/j.jes.2017.03.024

    Article  Google Scholar 

  72. Hoefman S, van der Ha D, Boon N, Vandamme P, De Vos P, Heylen K (2014) Niche differentiation in nitrogen metabolism among methanotrophs within an operational taxonomic unit. BMC Microbio 14:83. https://doi.org/10.1186/1471-2180-14-83

    Article  Google Scholar 

  73. Damm E, Kiene RP, Schwarz J, Falck E, Dieckmann G (2008) Methane cycling in Arctic shelf water and its relationship with phytoplankton biomass and DMSP. Mar Chem 109:45–59. https://doi.org/10.1016/j.marchem.2007.12.003

    Article  CAS  Google Scholar 

  74. Jorgensen BB (1977) Bacterial sulphate reduction within reduced microniches of oxidized marine sediments. Mar Biol 41:7–17. https://doi.org/10.1007/BF00390576

    Article  Google Scholar 

  75. Fry JC (1987) Functional roles of the major groups of bacteria associated with detritus. In: DJW M, Pullin RSV (eds) Detritus and Microbial Ecology in Aquaculture. ICLARM Conference Proceedings, Manila, pp 83–122

    Google Scholar 

  76. Hu X, Liu J, Liu H, Zhuang G, Xun L (2018) Sulfur metabolism by marine heterotrophic bacteria involved in sulfur cycling in the ocean. Sci China Earth Sci 61:1369–1378. https://doi.org/10.1007/s11430-017-9234-x

    Article  CAS  Google Scholar 

  77. Li Y, Tang K, Zhang L, Zhao Z, Xie X, Chen CTA, Wang D, Jiao N, Zhang Y (2018) Coupled carbon, sulfur, and nitrogen cycles mediated by microorganisms in the water column of a shallow-water hydrothermal ecosystem. Front Microbio l9:2718. https://doi.org/10.3389/fmicb.2018.02718

    Article  Google Scholar 

  78. Hoehler TM, Alperin MJ, Albert DB, Martens CS (1994) Field and laboratory studies of methane oxidation in an anoxic marine sediment: evidence for a methanogen–sulfate reducer consortium. Glob Biogeochem Cycles 8:451–463. https://doi.org/10.1029/94GB01800

    Article  CAS  Google Scholar 

  79. Fdz-Polanco F, Fdz-Polanco M, Fernandez N, Urueña MA, Garcia PA, Villaverde S (2001) New process for simultaneous removal of nitrogen and sulphur under anaerobic conditions. Water Res 35:1111–1114. https://doi.org/10.1016/S0043-1354(00)00474-7

    Article  CAS  PubMed  Google Scholar 

  80. Bao P, Li GX, Sun GX, Xu YY, Meharg AA, Zhu YG (2018) The role of sulfate-reducing prokaryotes in the coupling of element biogeochemical cycling. Sci Total Environ 613:398–408. https://doi.org/10.1016/j.scitotenv.2017.09.062

    Article  CAS  PubMed  Google Scholar 

  81. Furtado PS, Campos BR, Serra FP, Klosterhoff M, Romano LA, Wasielesky W (2015) Effects of nitrate toxicity in the Pacific white shrimp, Litopenaeus vannamei, reared with biofloc technology (BFT). Aquacult Int 23:315–327. https://doi.org/10.1007/s10499-014-9817-z

    Article  CAS  Google Scholar 

  82. Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105:11512–11519. https://doi.org/10.1073/pnas.0801925105

    Article  PubMed  PubMed Central  Google Scholar 

  83. Xiong J, Zhu J, Wang K, Wang X, Ye X, Liu L, Zhao Q, Hou M, Qiuqian L, Zhang D (2014) The temporal scaling of bacterioplankton composition: high turnover and predictability during shrimp cultivation. Microb Ecol 67:256–264. https://doi.org/10.1007/s00248-013-0336-7

    Article  PubMed  Google Scholar 

  84. Zhang D, Wang X, Xiong J, Zhu J, Wang Y, Zhao Q, Chen H, Guo A, Wu J, Dai H (2014) Bacterioplankton assemblages as biological indicators of shrimp health status. Ecol Indic 38:218–224. https://doi.org/10.1016/j.ecolind.2013.11.002

    Article  CAS  Google Scholar 

  85. Qin Y, Hou J, Deng M, Liu Q, Wu C, Ji Y, He X (2016) Bacterial abundance and diversity in pond water supplied with different feeds. Sci Rep 6:35232. https://doi.org/10.1038/srep35232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Hou D, Huang Z, Zeng S, Liu J, Wei D, Deng X, Weng S, He Z, He J (2017) Environmental factors shape water microbial community structure and function in shrimp cultural enclosure ecosystems. Front Microbiol 8:2359. https://doi.org/10.3389/fmicb.2017.02359

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to acknowledge the Director, CSIR-National Institute of Oceanography (CSIR-NIO), for the facilities and encouragement. The authors would like to record the cooperation of the commercial shrimp farm for permitting the fieldwork. Thanks are also extended to anonymous reviewers for improving the quality of the manuscript. This is CSIR-NIO contribution Number 6580.

Funding

EAS acknowledges the University Grants Commission (UGC), India, for providing the Junior and Senior Research Fellowship (RF-83231). Council of Scientific and Industrial Research (CSIR) for funding the project (PSC 0206).

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Correspondence to Maria Judith Gonsalves.

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Sabu, E.A., Gonsalves, M.J., Sreepada, R.A. et al. Evaluation of the Physiological Bacterial Groups in a Tropical Biosecured, Zero-Exchange System Growing Whiteleg Shrimp, Litopenaeus vannamei. Microb Ecol 81, 335–346 (2021). https://doi.org/10.1007/s00248-020-01575-w

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