Abstract
This study examined the phylogenetic and metabolic features of microbial communities in Baisha Bay mariculture areas of Nan’ao Island, a mariculture base on the Chinese Guangdong coast. Large seaweed (Gracilaria lemaneiformis) cultivation zones (LZ), fish culture zones (FZ), and control zones (CZ) were sampled. According to community-level physiological profiling, d-mannitol, d-mannitol/α-d-lactose, and d-mannitol/α-cyclodextrin were the carbon sources with the highest utilization rates in CZ, LZ, and FZ, respectively (R s > 1.9). Denaturing gradient gel electrophoresis analysis showed that the dominant bacteria in CZ and LZ were Alphaproteobacteria (39.9 and 34.5%, respectively), whereas in FZ they were Flavobacteria (32.2%). The Shannon diversity in CZ and LZ was significantly higher than in FZ (P < 0.05). Some opportunistic pathogens, such as Vibrio, Pseudoalteromonas and Loktanella, were abundant in FZ. The microbial communities and most of the dominant bacteria in FZ were more affected by environmental factors including salinity, chemical oxygen demand and total phosphorus. Some bacteria, such as Brevundimonas and Polaribater, have the potential to degrade agar in seaweed, and were isolated from samples rich in algae which are dominant in LZ. The cultivation of G. lemaneiformis created the notable structures and functions of macroalgae-associated bacterial communities that were less affected by the environmental factors examined.
Similar content being viewed by others
References
Yang YF, Hou LC, Nie XP, Tang DL, Chung IK (2004) Development of mariculture and its impacts in Chinese coastal waters. Rev Fish Biol Fisher 14:1–10
Hong WS, Zhang QY (2003) Review of captive bred species and fry production of marine fish in China. Aquaculture 227:305–318
Li K, Liu LP, Clausen JH, Lu M, Dalsgaard A (2016) Management measures to control diseases reported by tilapia (Oreochromis spp.) and whiteleg shrimp (Litopenaeus vannamei) farmers in Guangdong, China. Aquaculture 457:91–99
Zhang JH, Hansen PK, Fang JG (2009) Assessment of the local environmental impact of intensive marine shellfish and seaweed farming-Application of the MOM system in the Sungo Bay, China. Aquaculture 287:304–310
Han QX, Wang YQ, Zhang Y, Keesing J, Liu DY (2013) Effects of intensive scallop mariculture on macrobenthic assemblages in Sishili Bay, the northern Yellow Sea of China. Hydrobiologia 718:1–15
Wang YB, Xu ZR, Xia MS (2005) The effectiveness of commercial probiotics in northern white shrimp Penaeus vannamei ponds. Fish Sci 71:1036–1041
Cao YC, Wen GL, Li ZJ, Liu XZ, Hu XJ, Zhang JS, He JG (2014) Effects of dominant microalgae species and bacterial quantity on shrimp production in the final culture season. J Appl Phycol 26:1749–1757
Troll M, Hallling C, Nero A, Chopin T, Buschmann AH, Kautsky N, Yarish C (2003) Integrated mariculture: asking the right questions. Aquaculture 226:69–90
Wu R (1995) The environmental impact of marine fish culture: towards a sustainable future. Mar Pollut Bull 31:159–166
Yang YF, Chai ZY, Wang Q, Chen WZ, He ZL, Jiang SJ (2015) Cultivation of seaweed Gracilaria in Chinese coastal waters and its contribution to environmental improvements. Algal Res 9:236–244
Zodape ST (2001) Seaweeds as a biofertilizer. J Sci Ind Res 60:378–382
Gu YG, Yang YF, Lin Q, Li QS, Wang ZH, Wang X (2012) Spatial, temporal, and speciation variations of heavy metals in sediments of Nan’ao Island, a representative mariculture base in Guangdong coast, China. J Environ Monit 14:1943–1950
Lai XW, Chen WZ (2006) Progress and research on ecological mariculture in Nan’ao island. J Fish Sci Technol 2:33–34 (in Chinese)
Fei XG (2004) Solving the coastal eutrophication problem by large scale seaweed cultivation. Hydrobiologia 512:145–151
Yang YF, Fei XG, Song JM, Hu HY, Wang GC, Chung IK (2006) Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture 254:248–255
Schiff K, Luk B, Gregorio D, Gruber S (2011) Assessing water quality in Marine Protected Areas from Southern California, USA. Mar Pollut Bull 62:2780–2786
Wallace J, Stewart L, Hawdon A, Keen R, Karim F, Kemei J (2009) Flood water quality and marine sediment and nutrient loads from the Tully and Murray catchments in north Queensland, Australia. Mar Freshw Res 60:1123–1131
Paerl H, Dyble J, Twomey L, Pinckney J, Nelson J, Kerkhof L (2002) Characterizing man-made and natural modifications of microbial diversity and activity in coastal ecosystems. Antonie Van Leeuwenhoek 81:487–507
González JM, Simó R, Massana R, Covert JS, Casamayor EO, Pedrós-Alió C, Moran MA (2000) Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl Environ Microb 66:4237–4246
Zhang DM, Wang X, Xiong JB, Zhu JL, Wang YN, Zhao QF, Chen HP, Guo AN, Wu JF, Dai HP (2014) Bacterioplankton assemblages as biological indicators of shrimp health status. Ecol Indic 38:218–224
Yoza BA, Harada RM, Nihous GC, Li QX, Masytani SM (2007) Impact of mariculture on microbial diversity in sediments near open ocean farming of Polydactylus sexfilis. Ecol Indic 7:108–122
Crump BC, Armbrust EV, Baross JA (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia river, its estuary, and the adjacent coastal ocean. Appl Environ Microb 65:3192–3204
Stevens H, Ulloa O (2008) Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ Microbiol 10:1244–1259
Liu ZH, Huang SB, Sun GP, Xu ZC, Xu MY (2012) Phylogenetic diversity, composition and distribution of bacterioplankton community in the Dongjiang River, China. FEMS Microbiol Ecol 80:30–44
Sekiguchi H, Koshikawa H, Hiroki M, Murakami S, Xu K, Watanabe M, Nakahara T, Zhu M, Uchiyama H (2002) Bacterial distribution and phylogenetic diversity in the Changjiang estuary before the construction of the Three Gorges Dam. Microb Ecol 43:82–91
Blancheton JP, Attramadal KJK, Michaud L, d’Orbcastel ER, Vadstein O (2013) Insight into bacterial population in aquaculture systems and its implication. Aquacult Eng 53:30–39
Tamminen M, Karkman A, Corander J, Paulin L, Virta M (2011) Differences in bacterial community composition in Baltic Sea sediment in response to fish farming. Aquaculture 313:15–23
Sakami T, Fujioka Y, Shimoda T (2008) Comparison of microbial community structures in intensive and extensive shrimp culture ponds and a mangrove area in Thailand. Fish Sci 74(4):889–898
Kirk JL, Klironomos JN, Lee H, Trevors JT (2005) The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environ Pollut 133:455–465
Lee EH, Kim J, Kim JY, Koo SY, Lee SD, Ko KS, Ko DC, Yum BY, Cho KS (2010) Comparison of microbial communities in petroleum-contaminated groundwater using genetic and metabolic profiles at Kyonggi-Do, South Korea. Environ Earth Sci 60:371–382
GB/T 12763.4-2007 Specifications for oceanographic survey-Part 4: survey of chemical parameters in sea water, National Standards of the P.R.C. compositions. Biogeosciences. 7: 3343–3362 (in Chinese)
APHA (American Public Health Association) (1998) Standard methods for the examination of water and waste water, 20th edn. Am Public Health Assoc, Washington, DC
Weber KP, Legge RL (2011) Dynamics in the bacterial community-level physiological profiles and hydrological characteristics of constructed wetland mesocosms during start-up. Ecol Eng 37:666–677
Choi KH, Dobbs FC (1999) Comparison of two kinds of Biolog microplates (GN and ECO) in their ability to distinguish among aquatic microbial communities. J Microbiol Methods 36:203–213
Khalil S, Alsanius BW (2009) Utilisation of carbon sources by Pythium, Phytophthora and Fusarium Species as determined by Biolog® microplate assay. Open Microbiol J 3:9–14
Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level, sole-carbon-source utilization. Appl Environ Microb 57:2351–2359
Xi JY, Hu HY, Jiang J, Qian Y (2005) Metabolic properties of the microbial community in the biofilters using biolog microplates. Environ Sci 26:165–170 (in Chinese with English abstract)
Yang YF, Hu XJ, Zhang J, Gong YX (2013) Community level physiological study of algicidal bacteria in the phycosphere of Skeletonema costatum and Scrippsiella trochoidea. Harmful Algae 28:88–96
Muyzer G, De-Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Moss A, Bassall M (2006) Effects of disturbance on the biodiversity and abundance of isopods in temperature grasslands. Eur J Soil Biol 42:S254–S268
Hu XJ, Liu Q, Li ZJ, He ZL, Gong YX, Cao YC, Yang YF (2014) Metabolic and phylogenetic profiles of microbial communities in Guishan Island of South China Sea. J Ocean Univ China 13:857–864
TerBraak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: Software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca
Kirchman DL, Meon B, Ducklow HW, Carlson CA, Hansell DA, Steward GF (2001) Glucose fluxes and concentrations of dissolved combined neutral sugars (polysaccharides) in the Ross Sea and Polar Front Zone, Antarctica. Deep Sea Res Part 2 Top Stud Oceanogr 48:4179–4197
Hernes PJ, Hedges JI, Peterson ML, Wakeham SG, Lee C (1996) Neutral carbohydrate geochemistry of particulate material in the central equatorial Pacific. Deep Sea Res Part Top Stud Oceanogr 43:1181–1204
He B, Dai M, Huang W, Liu Q, Chen H, Xu L (2010) Sources and accumulation of organic carbon in the Pearl River Estuary surface sediment as indicated by elemental, stable carbon isotopic, and carbohydrate compositions. Biogeosciences 7:3343–3362
Rohani-Ghadikolaei K, Abdulalian E, Ng W-K (2012) Evaluation of the proximate, fatty acid and mineral composition of representative green, brown and red seaweeds from the Persian Gulf of Iran as potential food and feed resources. J Food Sci Technol 49(6):774–780
Groisillier A, Labourel A, Michel G, Tonon T (2015) The mannitol utilization system of the marine bacterium Zobellia galactanivorans. Appl Environ Microbiol 81(5):1790–1803
Lu KG, Wei L, Liu JG (2008) The characteristics of nutrient removal and inhibitory effect of Ulva clathrata on Vibrio anguillarum 65. J Appl Phycol 20:1061–1068
Fandino LB, Riemann L, Steward GF, Long RA, Azam F (2001) Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquat Microb Ecol 23:119–130
Wada M, Mori F, Yokouchi K, Yagi M, Takita T, Ishimatsu A, Iwataki M, Takahashi K, Van Mai H, Thanh Vo T, Phuoc Ha H, Dac Tran D (2016) Comparison of planktonic microbial abundance and dissolved oxygen consumption between the aquaculture ponds of mudskippers and shrimps in the Mekong Delta, southern Vietnam. Fish Sci 82(5):787–797
Bonilla-Findji O, Herndl GJ, Gattuso JP, Weinbauer MG (2009) Viral and flagellate control of prokaryotic production and community structure in offshore Mediterranean waters. Appl Environ Microb 75:4801–4812
Balcázar JL, Lee NM, Pintado J, Planas M (2010) Phylogenetic characterization and in situ detection of bacterial communities associated with seahorses (Hippocampus guttulatus) in captivity. Syst Appl Microbiol 33:71–77
Planas M, Pérez-Lorenzo M, Hjelm M, Gram L, Fiksdal IU, Bergh Ø, Pintado J (2006) Probiotic effect in vivo of Roseobacter strain 27-4 against Vibrio (Listonella) anguillarum infections in turbot (Scophthalmus maximus L.) larvae. Aquaculture 255:323–333
Li SQ, Pan JL, Li ZH, Liu XL, Tan J, Yang H (2014) Characterization of an algicidal bacterium Brevundimonas J4 and chemical defense of Synechococcus sp. BN60 against bacterium J4. Harmful Algae 37:1–7
Fukui Y, Abe M, Kobayashi M, Saito H, Oikawa H, Yano Y, Satomi M (2013) Polaribacter porphyrae sp. nov., isolated from the red alga Porphyra yezoensis, and emended descriptions of the genus Polaribacter and two Polaribacter species. Int J Syst Evol Microbiol 63:1665–1672
She BJ, Tao XQ, Huang T, Lu GN, Zhou ZL, Guo CL, Dang Z (2016) Effects of nano bamboo charcoal on PAHs-degrading strain Sphingomonas sp. GY2B. Ecotox Environ Safe 125:35–42
Austin B, Zhang XH (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43:119–124
Hubbard TP, Chao MC, Abel S, Blondel CJ, Abel Zur Wiesch P, Zhou X, Davis BM, Waldor MK (2016) Genetic analysis of Vibrio parahaemolyticus intestinal colonization. Proc Natl Acad Sci USA 113(22):6283–6288
Choudhury JD, Pramanik A, Webster NS, Llewellyn LE, Gachhui R, Mukherjee J (2015) The pathogen of the great barrier reef sponge Rhopaloeides odorabile is a new strain of Pseudoalteromonas agarivorans containing abundant and diverse virulence-related genes. Mar Biotechnol 17:463–478
Mancuso FP, D’hondt S, Willems A, Airoldi v, De Clerck O (2016) Diversity and Temporal Dynamics of the Epiphytic Bacterial Communities Associated with the Canopy-Forming Seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin. Front Microbial 7:476
Liu JJ, Chen QZ, Zeng JN, Gao AG, Liao YB (2006) Studies on the ecology of microorganisms in maricultural areas. J Zhejiang Ocean Univ (Natural Sci) 25:72–77 (in Chinese with English abstract)
Nero A, Chopin T, Troll M, Buschmann AH, Kraemer P, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391
Pang SJ, Xiao T, Bao Y (2006) Dynamic changes of total bacteria and Vibrio in an integrated seaweed-abalone culture system. Aquaculture 252:289–297
Skriptsova AV, Miroshnikova NV (2011) Laboratory experiment to determine the potential of two macroalgae from the Russian Far-East as biofilters for integrated multi-trophic aquaculture (IMTA). Bioresour Technol 102:3149–3154
Acknowledgements
This research was supported by the Joint Project of the Nature Science Foundation of China-Guangdong (U1301235), the Chinese Special Fund for Agro-scientific Research in the Public Interest (201403008), the Fund of the Key Laboratory of South China Sea Fishery Resources Exploitation & Utilization, the Ministry of Agriculture, P. R. China (FREU2015-08), and the Natural Science Foundation of Hainan Province (20163148).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
None.
Rights and permissions
About this article
Cite this article
Hu, X., Wen, G., Cao, Y. et al. Metabolic and phylogenetic profiles of microbial communities from a mariculture base on the Chinese Guangdong coast. Fish Sci 83, 465–477 (2017). https://doi.org/10.1007/s12562-017-1073-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-017-1073-5