Abstract
In mangrove environments, bacterioplankton communities constitute an important component of aquatic biota and play a major role in ecosystem processes. Variability of bacterioplankton communities from Sundarbans mangrove, located in the Indian subcontinent in South Asia and sits on the apex of Bay of Bengal, was investigated over monsoon and post-monsoon seasons. The study was undertaken in two stations in Sundarbans using 16S rRNA clone library and Illumina MiSeq approaches with focus on the functionally important members that participate in coastal biogeochemical cycling. Out of 544 sequenced clones, Proteobacteria dominated the study area (373 sequences) with persistence of two major classes, namely, Gammaproteobacteria and Alphaproteobacteria across both monsoon and post-monsoon seasons in both stations. Several sequences belonging to Sphingomonadales, Chromatiales, Alteromonadales, Oceanospirillales, and Bacteroidetes were encountered that are known to play important roles in coastal carbon cycling. Some sequences showed identity with published uncultured Planctomycetes and Chloroflexi highlighting their role in nitrogen cycling. The detection of two novel clades highlighted the existence of indigenous group of bacterioplankton that may play important roles in this ecosystem. The eubacterial V3–V4 region from environmental DNA extracted from the above two stations, followed by sequencing in Illumina MiSeq system, was also targeted in the study. A congruency between the clone library and Illumina approaches was observed. Strong variability in bacterioplankton community structure was encountered at a seasonal scale in link with precipitation. Drastic increase in sediment associated bacteria such as members of Firmicutes and Desulfovibrio was found in monsoon hinting possible resuspension of sediment-dwelling bacteria into the overlying water column. Principal component analysis (PCA) revealed dissolved ammonium and dissolved nitrate to account for maximum variation observed in the bacterioplankton community structure. Overall, the study showed that a strong interplay exists between environmental parameters and observed variability in bacterioplankton communities as a result of precipitation which can ultimately influence processes and rates linked to coastal biogeochemical cycles.
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Abbreviations
- 16S rRNA:
-
16S ribosomal ribonucleic acid
- SWT:
-
Surface water temperature
- DO:
-
Dissolved oxygen
- OTUs:
-
Operational taxonomic units
- NJ:
-
Neighbor joining
- PCA:
-
Principal component analysis
- NGS:
-
Next-generation sequencing
References
Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29(3):331–349. https://doi.org/10.1017/S0376892902000231
Alongi DM (2012) Carbon sequestration in mangrove forests. Carbon Manag 3:313–322. https://doi.org/10.4155/cmt1220
Alongi DM (2014) Carbon cycling and storage in mangrove forests. Annu Rev Mar Sci 6:195–219. https://doi.org/10.1146/annurev-marine-010213-135020
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25173389
Amalfitano S, Corno G, Eckert E, Fazi S, Ninio S, Callieri C, Grossart H-P, Eckert W (2017) Tracing particulate matter and associated microorganisms in freshwaters. Hydrobiologia 800(1):145–154. https://doi.org/10.1007/s10750-017-3260-x
Andreote FD, Jiménez DJ, Chaves D, Dias ACF, Luvizotto DM, Dini-Andreote F, Fasanella CC, Lopez MV, Baena S, Taketani RG, de Melo IS (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS ONE 7(6):e38600. https://doi.org/10.1371/journalpone0038600
Ansari MI, Harb M, Jones B, Hong PY (2015) Molecular-based approaches to characterize coastal microbial community and their potential relation to the trophic state of Red Sea. Sci Rep 5:9001. https://doi.org/10.1038/srep09001
Azam F, Long RA (2001) Oceanography: sea snow microcosms. Nature 414(6863):495–498. https://doi.org/10.1038/35107174
Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E, Würdemann CA, Quast C, Kuhl H, Knaust F, Woebken D, Bischof K, Mussmann M, Choudhuri JV, Meyer F, Reinhardt R, Amann RI, Glöckner FO (2006) Whole genome analysis of the marine Bacteroidetes ‘Gramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ Microbiol 8(12):2201–2213. https://doi.org/10.1111/j.1462-2920.2006.01152.x
Basak P, Pramanik A, Sengupta S, Nag S, Bhattacharyya A, Roy D, Pattanayak R, Ghosh A, Chattopadhyay D, Bhattacharyya M (2016) Bacterial diversity assessment of pristine mangrove microbial community from Dhulibhashani, Sundarbans using 16S rRNA gene tag sequencing. Genom Data 7:76–78. https://doi.org/10.1016/jgdata201511030
Bhattacharjee D, Samanta B, Danda AA, Bhadury P (2013) Temporal succession of phytoplankton assemblages in a tidal creek system of the Sundarbans mangroves—an integrated approach. Int J Biodivers 2013:1–15. https://doi.org/10.1155/2013/824543
Bianchi TS (2011) The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. PNAS 108(49):19473–19481. https://doi.org/10.1073/pnas.1017982108
Bostrӧm KH, Simu K, Hagstrӧm A, Riemann L (2004) Optimization of DNA extraction for quantitative marine bacterioplankton community analysis. Limnol Oceanogr Methods 2:365–373. https://doi.org/10.4319/lom20042365
Bouskill NJ, Eveillard D, O'Mullan G, Jackson GA, Ward BB (2011) Seasonal and annual reoccurrence in betaproteobacterial ammonia-oxidizing bacterial population structure. Environ Microbiol 13:872–886. https://doi.org/10.1111/j1462-2920201002362x
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
Chaudhuri K, Manna S, Sarma KS, Naskar P, Bhattacharyya S, Bhattacharyya M (2012) Physiochemical and biological factors controlling water column metabolism in Sundarbans estuary, India. Aquat Biosyst 8(1):26. https://doi.org/10.1186/2046-9063-8-26
Choudhury AK, Das M, Phillip P, Bhadury P (2015) An assessment of the implications of seasonal precipitation and anthropogenic influences on a mangrove ecosystem using phytoplankton as proxies. Estuar Coasts 38(3):854–872. https://doi.org/10.1007/s12237-014-9854-x
Choudhury A, Bhadury P (2015) Relationship between N: P: Si ratio and phytoplankton community composition in a tropical estuarine mangrove ecosystem. Biogeosci Discuss 12:2307–2355. https://doi.org/10.5194/bgd-12-2307-2015
Clarke KR, Gorley RN (2006) PRIMER (Plymouth routines in multivariate ecological research) v6: user manual/tutorial. PRIMER-E, Plymouth
Cottrell MT, Kirchman DL (2000) Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Appl Environ Microbiol 66(12):5116–5122. https://doi.org/10.1128/AEM.66.12.5116-5122.2000
Cottrell MT, Waidner LA, Yu L, Kirchman DL (2005) Bacterial diversity of metagenomic and PCR libraries from the Delaware River. Environ Microbiol 7:1883–1895. https://doi.org/10.1111/j1462-2920200500762x
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 Microbiol 65(7):3192–3204
Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505. https://doi.org/10.1128/AEM7031494-15052004
Díez-Vives C, Gasol JM, Acinas SG (2014) Spatial and temporal variability among marine Bacteroidetes populations in the NW Mediterranean Sea. Syst Appl Microbiol 37(1):68–78. https://doi.org/10.1016/jsyapm201308006
dos Santos HF, Cury JC, do Carmo FL, dos Santos AL, Tiedje J, van Elsas JD, Rosado AS, Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS ONE 6(3):e16943. https://doi.org/10.1371/journalpone0016943
Drummond AJ, Newcomb RD, Buckley TR, Xie D, Dopheide A, Potter BCM, Heled J, Ross HA, Tooman L, Grosser S, Park D, Demetras NJ, Stevens MI, Russell JC, Anderson SH, Carter A, Nelson N (2015) Evaluating a multigene environmental DNA approach for biodiversity assessment. GigaScience 4(1):46. https://doi.org/10.1186/s13742-015-0086-1
Ducklow HW, Carlson CA (1992) Oceanic bacterial production. In: Marshall KC (ed) Advances in microbial ecology, 12th edn. Plenum Press, New York, pp 113–181
Dworkin M, Falkow S (2006) The prokaryotes. Bacteria: Firmicutes, Cyanobacteria a handbook on the biology of bacteria. Springer, New York
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformaticsbtr381
Evans RD (1994) Empirical evidence of the importance of sediment resuspension in lakes. Hydrobiologia 284(1):5–12. https://doi.org/10.1007/BF00005727
Felsenstein J (2005) PHYLIP (phylogeny inference package) version 3.6. Distributed by author. Department of Genome Sciences, University of Washington, Seattle http://evolution.genetics.washington.edu/phylip.html
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 Ecol 70(2):80–92. https://doi.org/10.1111/j.1574-69411.2009.00772.x
Fernandes SO, Kirchman DL, Michotey VL, Bonin PC, LokaBharathi PA (2014) Bacterial diversity in relatively pristine and anthropogenically-influenced mangrove ecosystems (Goa, India). Braz J Microbiol 45(4):1161–1171. https://doi.org/10.1590/S1517-83822014000400006
Finch MS, Hydes DJ, Clayson CH, Weigl B, Dakin J, Gwilliam P (1998) A low power ultra violet spectrophotometer for measurement of nitrate in seawater: introduction, calibration and initial sea trials. Anal Chim Acta 377(2–3):167–177. https://doi.org/10.1016/S0003-2670 (98)00616-3
Fortunato CS, Crump BC (2015) Microbial gene abundance and expression patterns across a river to ocean salinity gradient. PLoS ONE 10(11):e0140578. https://doi.org/10.1371/journalpone0140578
Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci U S A 105(22):7774–7778. https://doi.org/10.1073/pnas.0803070105
Fukami K, Simidu U, Taga N (1985) Microbial decomposition of phyto- and zooplankton in seawater II—changes in the bacterial community. Mar Ecol Prog Ser 21:7–13. https://doi.org/10.3354/meps021007
Gattuso JP, Frankignoulle M, Wollast R (1998) Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu Rev Ecol Syst 29:405–434. https://doi.org/10.1146/annurevecolsys291405
Ghizelini AM, Mendonca-Hagler LC, Macrae A (2012) Microbial diversity in Brazilian mangrove sediments-a mini review. Braz J Microbiol 43(4):1242–1254. https://doi.org/10.1590/S1517-83822012000400002
Ghosh A, Dey N, Bera A, Tiwari A, Sathyaniranjan KB, Chakrabarti K, Chattopadhyay D (2010) Culture independent molecular analysis of bacterial communities in the mangrove sediment of Sundarbans, India. Saline Syst 6:1. https://doi.org/10.1186/1746-1448-6-1
Gomes NCM, Borges LR, Paranhos R, Pinto FN, Mendonça-Hagler LCS, Smalla K (2008) Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol Ecol 66(2008):96–109. https://doi.org/10.1111/j1574-6941200800519x
Gomes NC, Cleary DF, Calado R, Costa R (2011) Mangrove bacterial richness. Commun Integr Biol 4(4):419–423. https://doi.org/10.4161/cib4415253
Gouy M, Guindon S, Gascue O (2010) Seaview version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. https://doi.org/10.1093/molbev/msp259
Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98. https://doi.org/10.1021/bk-1999-0734ch008
Head IM, Jones DM, Rölling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4(3):173–182. https://doi.org/10.1038/nrmicro1348
He Q, Huang KH, He Z, Alm EJ, Fields MW, Hazen TC, Arkin AP, Wall JD, Zhou J (2006) Energetic consequences of nitrite stress in Desulfovibrio vulgaris Hildenborough, inferred from global transcriptional analysis. Appl Environ Microbiol 72:4370–4381. https://doi.org/10.1128/AEM02609-05
Henriques I, Almeida MA, Cunha MA, Correia A (2004) Molecular sequence analysis of prokaryotic diversity in the middle and outer sections of the Portuguese estuary Ria de Aveiro. FEMS Microbiol Ecol 49:269–279. https://doi.org/10.1016/jfemsec200404003
Herlemann DPR, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5(10):1571–1579. https://doi.org/10.1038/ismej.2011.41
Hewson I, Fuhrman JA (2004) Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol 70(6):3425–3433. https://doi.org/10.1128/AEM7063425-34332004
Hewson I, Steele JA, Capone DG, Fuhrman JA (2006) Temporal and spatial scales of variation in bacterioplankton assemblages of oligotrophic surface waters. Mar Ecol Prog Ser 311:67–77. https://doi.org/10.3354/meps311067
Hickey BM, Kudela RM, Nash JD, Bruland KW, Peterson WT, MacCready P et al (2010) River influences on shelf ecosystems: introduction and synthesis. J Geophys Res Oceans 115:C00B17. https://doi.org/10.1029/2009JC005452
Hollibaugh JT, Wong PS, Murrell MC (2000) Similarity of particle associated and free-living bacterial communities in northern San Francisco Bay, California. Aquat Microb Ecol 21:103–109. https://doi.org/10.3354/ame021103
Howlett ER, Bowers DG, Malarkey J, Jago CF (2015) Stratification in the presence of an axial convergent front: causes and implications. Estuar Coast Shelf Sci 161:1–10. https://doi.org/10.1016/j.ecss.2015.04.003
Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequences alignments. Bioinformatics 20:2317–2319. https://doi.org/10.1093/bioinformatics/bth226
Huse SM, Mark Welch DB, Voorhis A, Shipunova A, Morrison HG, Eren A, Sogin ML (2014) VAMPS: a website for visualization and analysis of microbial population structures. BMC Bioinf 15(1):41. https://doi.org/10.1186/1471-2105-15-41
Kirchman DL (2002) The ecology and Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39(2):91–100. https://doi.org/10.1111/j.1574-6941.2002.tb00910.x
Kirchman DL, Dittel AI, Malmstrom RR, Cottrell MT (2005) Biogeography of major bacterial groups in the Delaware Estuary. Limnol Oceanogr 50(5):167–1706
Kleeberg AM, Hupfer M, Gust G, Salka I, Pohlmann K, Grossart H-P (2013) Intermittent riverine resuspension: effects on phosphorus transformation and heterotrophic bacteria. Limno Oceanogr 58(2):635–652. https://doi.org/10.4319/lo.2013.58.2.0635
Laanbroek HJ, Keijzer RM, Verhoeven JTA, Whigham DF (2012) The distribution of ammonia-oxidizing betaproteobacteria in strands of Black mangroves (Avicennia germinans). Front Microbiol 3:153. https://doi.org/10.3389/fmicb201200153
Larsen A, Castberg T, Sandaa RA, Brussaard CPD, Egge J, Heldal M, Paulino A, Thyrhaug R, van Hannen EJ, Bratbak G (2001) Population dynamics and diversity of phytoplankton, bacteria and viruses in a seawater enclosure. Mar Ecol Prog Ser 221:47–57. https://doi.org/10.3354/meps221047
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley And Sons, New York, pp 115–175
Liao PC, Huang BH, Huang S (2007) Microbial community composition of the Danshui River Estuary of Northern Taiwan and the practicality of the phylogenetic method in microbial barcoding. Microb Ecol 54(3):497–507. https://doi.org/10.1007/s00248-007-9217-2
Liddicoat ML, Tibbitts S, Butler E (1975) The determination of ammonia in seawater. Limnol Oceanogr 20:131. https://doi.org/10.4319/lo19752010131
Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 104(27):11436–11440. https://doi.org/10.1073/pnas.0611525104
Manna S, Chaudhuri K, Bhattacharyya S, Bhattacharyya M (2010) Dynamics of Sundarbans estuarine ecosystem: eutrophication induced threat to mangroves. Saline Syst 6:8. https://doi.org/10.1186/1746-1448-6-8
Morris RM, Vergin KL, Cho JC, Rappe MS, Carlson CA, Giovannoni SJ (2005) Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic time-series study site. Limnol Oceanogr 50(5):1687–1696. https://doi.org/10.4319/lo.2005.50.5.1687
Motes ML, DePaola A, Cook DW, Veazey JE, Hunsucker JC, Garthright WE, Blodgett RJ, Chirtel SJ (1998) Influence of water temperature and salinity on Vibrio vulnificus in Northern Gulf and Atlantic coast oysters (Crassostrea virginica). Appl Environ Microbiol 64(4):1459–1465
Nealson KH (1997) Sediment bacteria: who’s there, what are they doing, and what's new? Annu Rev Earth Planet Sci 25(1):403–434. https://doi.org/10.1146/annurev.earth.25.1.403
Newell SY, Fell JW (1997) Competition among mangrove oomycetes, and between oomycetes and other microbes. Aquat Microb Ecol 12:21–28. https://doi.org/10.3354/ame012021
Nogales B, Aguiló-Ferretjans MM, Martín-Cardona C, Lalucat J, Bosch R (2007) Bacterial diversity, composition and dynamics in and around recreational coastal areas. Environ Microbiol 9(8):1913–1929. https://doi.org/10.1111/j.1462-2920.2007.01308.x
Pérez-Jiménez JR, Kerkhof LJ (2005) Phylogeography of sulphate-reducing bacteria among disturbed sediments, disclosed by analysis of the dissimilatory sulphite reductase genes (dsrAB). Appl Environ Microbiol 71:1004–1011. https://doi.org/10.1128/AEM7121004–1011205
Pires ACC, Clery DFR, Almeida A, Cunha A, Dealtry S, Mendonça-Hagler LCS, Smalla K, Gomes NC (2012) Denaturing gradient gel electrophoresis and barcoding pyrosequencing reveals unprecedented archaeal diversity in mangrove sediment and rhizophere samples. Appl Environ Microbiol 78:5520–5528. https://doi.org/10.1128/AEM.00386-12
Rappé MS, Vergin K, Giovannoni SJ (2000) Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiol Ecol 33:219–232. https://doi.org/10.1111/j1574-69412000tb00744x
Randa MA, Polz MF, Lim E (2004) Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Appl Environ Microbiol 70(9):5469–5476. https://doi.org/10.1128/AEM7095469-54762004
Ravot G, Magot M, Fardeau ML, Patel BK, Thomas P, Garcia JL, Ollivier B (1999) Fusibacter paucivorans gen. nov., sp. nov., an anaerobic, thiosulfate-reducing bacterium from an oil-producing well. Int J Syst Bacteriol 49(3):1141–1147. https://doi.org/10.1099/00207713-49-3-1141
Reichenbach H (1999) The order Cytophagales. In The prokaryotes, eds Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, 3rd edition, release 3.0. New York: Springer-Verlag, pp 549–591
Riemann L, Steward GF, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66(2):578–587. https://doi.org/10.1128/AEM662578–5872000
Samanta B, Bhadury P (2014) Analysis of diversity of chromophytic phytoplankton in a mangrove ecosystem using rbcL gene sequencing. J Phycol 50(2):328–340. https://doi.org/10.1111/jpy12163
Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506. https://doi.org/10.1128/AEM7131501-15062005
Seitzinger SP, Kroeze C (1998) Global distribution of nitrous oxide production and N inputs in freshwater and coastal marine ecosystems. Glob Biogeochem Cycles 12(1):93–113. https://doi.org/10.1029/97GB03657
Sekiguchi H, Watanabe M, Nakahara T, Xu B, Uchiyama H (2002) Succession of bacterial community structure along the Changjiang River determined by denaturing gradient gel electrophoresis and clone library analysis. Appl Environ Microbiol 68:5142–5150. https://doi.org/10.1128/AEM68105142-51502002
Selje N, Simon M (2003) Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany. Aquat Microb Ecol 30:221–237. https://doi.org/10.3354/ame030221
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539–544. https://doi.org/10.1038/msb.2011.75
Smith MW, Allen LZ, Allen AE, Herfort L, Simon HM (2013) Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem. Front Microbiol. https://doi.org/10.3389/fmicb201300120
Stahl DA, Fishbain S, Klein M, Baker BJ, Wagner M (2002) Origins and diversification of sulfate-respiring microorganisms. Antonie Van Leeuwenhoek 81(1–4):189–195. https://doi.org/10.1023/A:1020506415921
Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bull Fish Res Biodiversity Can 167:1–310
Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS One 9(8):e10559. https://doi.org/10.1371/journal.pone.0105592
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197
Teira E, Martinez-Garcia S, Lønborg C, Álvarez-Salgado XA (2009) Growth rates of different phylogenetic bacterioplankton groups in a coastal upwelling system. Environ Microbiol Rep 1(6):545–554. https://doi.org/10.1111/j1758-2229200900079x
Teira E, Martínez-García S, Lønborg C, Álvarez-Salgado XA (2011) Betaproteobacteria growth and nitrification rates during long-term natural dissolved organic matter decomposition experiments. Aquat Microb Ecol 63:19–27. https://doi.org/10.3354/ame01491
Trott LA, Alongi DM (2000) The impact of shrimp pond effluent on water quality and phytoplankton biomass in a tropical mangrove estuary. Mar Poll Bull 40(11):947–951. https://doi.org/10.1016/S0025-326X(00)00035-7
Troussellier M, Schafer H, Batailler N, Bernard L, Courties C, Lebaron P, Muyzer G, Servais P, Vives-Rego J (2002) Bacterial activity and genetic richness along an estuarine gradient (Rhone River plume, France). Aquat Microb Ecol 28:13–24. https://doi.org/10.3354/ame028013
Valiela I, Browen JL, York JK (2001) Mangrove forests: one of the world’s threatened major tropical environments. Biosciences 51(10):807–815. https://doi.org/10.1641/0006-3568 (2001)051[0807:MFOOTW]20CO;2
Vieira RP, Gonzalez AM, Cardoso AM, Oliveira DN, Albano RM, Clementino MM, Martins OB, Paranhos R (2008) Relationships between bacterial diversity and environmental variables in a tropical marine environment, Rio de Janeiro. Environ Microbiol 10(0):189–199. https://doi.org/10.1111/j.1462-2920.2007.01443.x
Waidner LA, Kirchman DL (2007) Aerobic anoxygenic phototrophic bacteria attached to particles in turbid waters of the Delaware and Chesapeake estuaries. Appl Environ Microbiol 73(12):3936–3944. https://doi.org/10.1128/AEM00592-07
Widdel F, Hansen TA (1999) The dissimilatory sulfate- and sulfur-reducing bacteria. In: Dworkin M, Schleifer KH, Stackebrandt E (eds) The prokaryotes: an evolving electronic database for the microbiological community, 3rd edn. Springer-Verlag, New York
Wright AC, Hill RT, Johnson JA, Roghman MC, Colwell RR, Morris JG (1996) Distribution of Vibrio vulnificus in the Chesapeake Bay. Appl Environ Microbiol 62(2):717–724
Wu XL, Yu SL, Gu J, Zhao GF, Chi CQ (2009) Filomicrobium insigne sp nov, isolated from an oil-polluted saline soil. Int J Syst Evol Microbiol 59:300–305. https://doi.org/10.1099/ijs0065758-0
Xue D, Boeckx P, Wang Z (2014) Nitrate sources and dynamics in a salinized river and estuary- a δ15N–NO3 − and δ18O–NO3 − isotope approach. Biogeosciences 11:5957–5967. https://doi.org/10.5194/bg-11-5957-2014
Yeo SK, Huggett MJ, Eiler A, Rappé MS (2013) Coastal bacterioplankton community dynamics in response to a natural disturbance. PLoS ONE 8(2):e56207. https://doi.org/10.1371/journal.pone.0056207
Zwolsman JJG (1994) Seasonal variability and biogeochemistry of phosphorus in the Scheldt Estuary, South-West Netherlands. Estuar Coast Shelf Sci 39(3):227–248. https://doi.org/10.1006/ecss.1994.1061
Acknowledgements
The authors thank the anonymous reviewers for their helpful suggestions.
Funding
Anwesha Ghosh is the recipient of IISER Kolkata Integrated Ph.D. Fellowship. This work is partly supported by grants from IISER Kolkata as well as from WWF-India awarded to Punyasloke Bhadury.
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P.B. designed the experiments. A.G. performed the experiments and analyzed the datasets. Both the authors wrote the manuscript.
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Responsible editor: Robert Duran
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Fig. S1
(a)-(j): Neighbour Joining (NJ) tree showing the phylogenetic position of the generated clones along with reference sequences taken from GenBank/DDBJ/EMBL databases. The NJ tree shows 544 clones representing Stn1 and Stn3. Number of identical clones have been shown in brackets. Methanobrevibacter smittii ATCC 35061 (NR044786) has been used as outgroup. Kimura-2-parameter with Gamma distribution was set as parameter for the NJ tree. Clone libraries representing a particular month from both stations have been given a specific colour for visualization purposes. (JPEG 268 kb)
Fig. S2
Rarefaction curve of combined 16S rRNA sequences for Stn1 and Stn3 during monsoon, post-monsoon and all seasons combined (JPEG 5 kb)
Fig. S3
Non-metric multidimensional scaling (nMDS) plot using Bray-Curtis distance for the bacterioplankton communities observed in each station and each month. (PNG 38 kb)
Fig S4
Rarefaction curves (at family level) show the sampling effort for Stn1_July_Il and Stn3_July_Il Illumina datasets (JPEG 3 kb)
Table S1
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Table S2
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Table S3
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Table S4
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Ghosh, A., Bhadury, P. Investigating monsoon and post-monsoon variabilities of bacterioplankton communities in a mangrove ecosystem. Environ Sci Pollut Res 25, 5722–5739 (2018). https://doi.org/10.1007/s11356-017-0852-y
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DOI: https://doi.org/10.1007/s11356-017-0852-y