Environmental Science and Pollution Research

, Volume 26, Issue 4, pp 3893–3908 | Cite as

Spatial and temporal heterogeneity in the structure and function of sediment bacterial communities of a tropical mangrove forest

  • Pratiksha Behera
  • Madhusmita Mohapatra
  • Ji Yoon Kim
  • Tapan K. Adhya
  • Ajit K. Pattnaik
  • Gurdeep RastogiEmail author
Research Article


Bacterial communities of mangrove sediments are well appreciated for their role in nutrient cycling. However, spatiotemporal variability in these communities over large geographical scale remains understudied. We investigated sediment bacterial communities and their metabolic potential in an intertidal mangrove forest of India, Bhitarkanika, using high-throughput sequencing of 16S rRNA genes and community-level physiological profiling. Bulk surface sediments from five different locations representing riverine and bay sites were collected over three seasons. Seasonality largely explained the variation in the structural and metabolic patterns of the sediment bacterial communities. Freshwater Actinobacteria were more abundant in monsoon, whereas γ-Proteobacteria demonstrated higher abundance in summer. Distinct differences in the bacterial community composition were noted between riverine and bay sites. For example, salt-loving marine bacteria affiliated to Oceanospirillales were more prominent in the bay sites than the riverine sites. l-asparagine, N-acetyl-d-glucosamine, and d-mannitol were the preferentially utilized carbon sources by bacterial communities. Bacterial community composition was largely governed by salinity and organic carbon content of the sediments. Modeling analysis revealed that the abundance of δ-Proteobacteria increased with salinity, whereas β-Proteobacteria displayed an opposite trend. Metabolic mapping of taxonomic data predicted biogeochemical functions such as xylan and chitin degradation, ammonia oxidation, nitrite reduction, and sulfate reduction in the bacterial communities suggesting their role in carbon, nitrogen, and sulfur cycling in mangrove sediments. This study has provided valuable clues about spatiotemporal heterogeneity in the structural and metabolic patterns of bacterial communities and their environmental determinants in a tropical mangrove forest.


Mangrove forest Bhitarkanika Bacterial communities Spatiotemporal heterogeneity 



The support received from the “ASM-IUSSTF Indo-US Professorship in Microbiology” awarded to Dr. G. Rastogi is also acknowledged. PCCF, Wild Life (Odisha), DFO-Rajnagar and mangrove forest division, Bhitarkanika Wildlife Sanctuary, and National Park are acknowledged for providing logistical help during field study. Authors sincerely appreciate the efforts of Mr. Bhagirathi Maharana for collecting the sediment samples from Bhitarkanika. The authors would like to acknowledge Mr. Bibhuti Bhusan Dora Research Fellow of GIS cell, Chilika Development Authority for the preparation of the sampling map. The Resourcesat-2 LISS III satellite image was obtained from the National Remote Sensing Center (NRSC), Hyderabad (India). Authors sincerely appreciate the constructive comments received from reviewers that helped improve the quality of this manuscript.

Funding information

This work was supported by the World Bank grant no. (Credit No. 4765-IN) given to Chilika Development Authority under the Integrated Coastal Zone Management Project (ICZMP) of Odisha.

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  1. Al-Amoudi S, Razali R, Essack M, Amini MS, Bougouffa S, Archer JAC, Lafi FF, Bajic VB (2016) Metagenomics as a preliminary screen for antimicrobial bioprospecting. Gene 594:248–258CrossRefGoogle Scholar
  2. Alzubaidy H, Essack M, Malas TB, Bokhari A, Motwalli O, Kamanu FK, Jamhor SA, Mokhtar NA, Antunes A, Simões MF, Alam I, Bougouffa S, Lafi FF, Bajic VB, Archer JAC (2016) Rhizosphere microbiome metagenomics of gray mangroves (Avicennia marina) in the Red Sea. Gene 576:626–636CrossRefGoogle Scholar
  3. 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:e38600CrossRefGoogle Scholar
  4. Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, Sinelnikov I, Budwill K, Nesbo CL, Wishart DS (2012) METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic Acids Res. 40:W88–W95CrossRefGoogle Scholar
  5. Atwood TB, Connolly RM, Almahasheer H, Carnell PE, Duarte CM, Lewis CJE, Irigoien X, Kelleway JJ, Lavery PS, Macreadie PI, Serrano O, Sanders CJ, Santos I, Steven ADL, Lovelock CE (2017) Global patterns in mangrove soil carbon stocks and losses. Nat Clim Change 7:523–528CrossRefGoogle Scholar
  6. Basak P, Majumder NS, Nag S, Bhattacharyya A, Roy D, Chakraborty A, SenGupta S, Roy A, Mukherjee A, Pattanayak R, Ghosh A, Chattopadhyay D, Bhattacharyya M (2015) Spatiotemporal analysis of bacterial diversity in sediments of Sundarbans using parallel 16S rRNA gene tag sequencing. Microb Ecol 69:500–511CrossRefGoogle Scholar
  7. Basak P, Pramanik A, Sengupta S, Nag S, Bhattacharyya A, Pattanayak R, Ghosh A, Chattopadhyay D, Roy D, Bhattacharyya M (2016) Bacterial diversity assessment of pristine mangrove microbial community from Dhulibhashani, Sundarbans using 16S rRNA gene tag sequencing. Genom Data 7:76–78CrossRefGoogle Scholar
  8. Behera P, Mahapatra S, Mohapatra M, Kim JY, Adhya TK, Raina V, Suar M, Pattnaik AK, Rastogi G (2017) Salinity and macrophyte drive the biogeography of the sedimentary bacterial communities in a brackish water tropical coastal lagoon. Sci Total Environ 595:472–485CrossRefGoogle Scholar
  9. Behera P, Mohapatra M, Adhya TK, Suar M, Pattnaik AK, Rastogi G (2018) Structural and metabolic diversity of rhizosphere microbial communities of Phragmites karka in a tropical coastal lagoon. Appl. Soil Ecol. 125:202–212CrossRefGoogle Scholar
  10. Bhomia RK, MacKenzie RA, Murdiyarso D, Sasmito SD, Purbopuspito J (2016) Impacts of land use on Indian mangrove forest carbon stocks: implications for conservation and management. Ecol. Appl. 26:1396–1408CrossRefGoogle Scholar
  11. Bouillon S, Moens T, Koedam N, Dahdouh-Guebas F, Baeyens W, Dehairs F (2004) Variability in the origin of carbon substrates for bacterial communities in mangrove sediments. FEMS Microbiol. Ecol. 49:171–179CrossRefGoogle Scholar
  12. Chauhan R, Ramanathan AL (2008) Evaluation of water quality of Bhitarkanika mangrove system, Orissa, east coast of India. Indian J Mar Sci 37:153–158Google Scholar
  13. Chen Q, Zhao Q, Li J, Jian S, Ren H (2016) Mangrove succession enriches the sediment microbial community in South China. Sci Rep 6:27468CrossRefGoogle Scholar
  14. Chen WC, Tseng WN, Hsieh JL, Wang YS, Wang SL (2010) Biodegradation and microbial community changes upon shrimp shell wastes amended in mangrove river sediment. J Environ Sci Health B 45:473–477CrossRefGoogle Scholar
  15. Dastgheib SM, Amoozegar MA, Khajeh K, Shavandi M, Ventosa A (2012) Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl Microbiol Biotechnol 95:789–798CrossRefGoogle Scholar
  16. Dias AC, Pereira e Silva MEC, Cotta SR, Dini-Andreote F, Soares FL Jr, Salles JF, Azevedo JL, van Elsas JD, Andreote D (2012, 2012) Abundance and genetic diversity of nifH gene sequences in anthropogenically affected Brazilian mangrove sediments. Braz J Microbial:653–660Google Scholar
  17. Dias ACF, Andreote FD, Rigonato J, Fiore FM, Melo IS, Araújo WL (2010) The bacterial diversity in a Brazilian non-disturbed mangrove sediment. Antonie Van Leeuwenhoek 98:541–551CrossRefGoogle Scholar
  18. 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:e16943CrossRefGoogle Scholar
  19. Duke NC, Meynecke JO, Dittmann S, Ellison AM, Anger K, Berger U, Cannicci S, Diele K, Ewel KC, Field CD, Koedam N, Lee SY, Marchand C, Nordhaus I, Dahdouh-Guebas F (2007) A world without mangroves? Science 317:41–42CrossRefGoogle Scholar
  20. Garland JL (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilisation. Soil Biol Biochem 28:213–221CrossRefGoogle Scholar
  21. Ghizelini AM, Mendonça-Hagler LCS, Macrae A (2012) Microbial diversity in Brazilian mangrove sediments – a mini review. Braz J Microbiol 43:4CrossRefGoogle Scholar
  22. 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 Sundarban, India. Saline Sys 6:1CrossRefGoogle Scholar
  23. 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 66:96–109CrossRefGoogle Scholar
  24. Gomes NCM, Flocco CG, Costa R, Junca H, Vilchez R, Pieper DH, Krögerrecklenfort E, Paranhos R, Mendonça-Hagler LCS, Smalla K (2010) Mangrove microniches determine the structural and functional diversity of enriched petroleum hydrocarbon-degrading consortia. FEMS Microbiol Ecol 74:276–290CrossRefGoogle Scholar
  25. Gutierrez T, Aitken MD (2014) Role of methylotrophs in the degradation of hydrocarbons during the Deepwater Horizon oil spill. ISME J. 8:2543–2545CrossRefGoogle Scholar
  26. Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganism in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fertil Soil 33:265–278CrossRefGoogle Scholar
  27. Ikenaga M, Guevara R, Dean AL, Pisani C, Boyer JN (2010) Changes in community structure of sediment bacteria along the Florida coastal everglades marsh–mangrove–seagrass salinity gradient. Microb Ecol 59:284–295CrossRefGoogle Scholar
  28. Imchen M, Kumavath R, Barh D, Vaz A, Góes-Neto A, Tiwari S, Ghosh P, Wattam AR, Azevedo V (2018) Comparative mangrove metagenome reveals global prevalence of heavy metals and antibiotic resistome across different ecosystems. Sci Rep 8:11187CrossRefGoogle Scholar
  29. Jacquiod S, Franqueville L, Cécillon SM, Vogel T, Simonet P (2013) Soil bacterial community shifts after chitin enrichment: an integrative metagenomic approach. PLoS One 8:e79699CrossRefGoogle Scholar
  30. Jiang XT, Peng X, Deng GH, Sheng HF, Wang Y, Zhou HW (2013) Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb Ecol 66:96–104CrossRefGoogle Scholar
  31. Jurelevicius D, Alvarez VM, Marques JM, de Sousa Lima LR, Dias Fde A, Seldin L (2013) Bacterial community response to petroleum hydrocarbon amendments in freshwater, marine, and hypersaline water-containing microcosms. Appl Environ Microbiol 79:5927–5935CrossRefGoogle Scholar
  32. Leboulanger C, Agogué H, Bernard C, Bouvy M, Carré C, Cellamare M, Duval C, Fouilland E, Got P, Intertaglia L, Lavergne C, Floćh EL, Roques C, Sarazin G (2017) Microbial diversity and cyanobacterial production in Dziani Dzaha Crater Lake, a unique tropical thalassohaline environment. PLoS One 12:e0168879CrossRefGoogle Scholar
  33. Li M, Cao H, Hong Y, Gu JD (2011) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl Microbiol Biotechnol 89:1243–1254CrossRefGoogle Scholar
  34. Liu M, Cui Y, Chen Y, Lin X, Huang H, Bao S (2016) Diversity of bacillus-like bacterial community in the sediments of the Bamenwan mangrove wetland in Hainan, China. Can J Microbiol 63:238–245CrossRefGoogle Scholar
  35. Liu Z, Frigaard NU, Vogl K, Iino T, Ohkuma M, Overmann J, Bryant DA (2012) Complete genome of Ignavibacterium album, a metabolically versatile, flagellated, facultative anaerobe from the phylum Chlorobi. Front Microbiol. 3:185Google Scholar
  36. Loganathachetti SD, Sadaiappan B, Poosakkannu A, Muthuraman S (2016) Pyrosequencing-based seasonal observation of prokaryotic diversity in pneumatophore-associated soil of Avicennia marina. Curr Microbiol 72:68CrossRefGoogle Scholar
  37. Mendes LM, Tsai SM (2017) Distinct taxonomic and functional composition of soil microbiomes along the gradient forest-restinga-mangrove in southeastern Brazil. Antonie van Leeuwenhoek 111:101–114CrossRefGoogle Scholar
  38. Mishra RR, Prajapati S, Das J, Dangar TK, Das N, Thatoi H (2011) Reduction of selenite to red elemental selenium by moderately halotolerant Bacillus megaterium strains isolated from Bhitarkanika mangrove soil and characterization of reduced product. Chemosphere 84:1231–1237CrossRefGoogle Scholar
  39. Mishra RR, Swain MR, Dangar TK, Thatoi H (2012) Diversity and seasonal fluctuation of predominant microbial communities in Bhitarkanika, a tropical mangrove ecosystem in India. Int J Trop Biol 60:909–924Google Scholar
  40. Ottoni JR, Cabral L, de Sousa STP, Lacerda Júnior GV, Domingos DF, Soares Junior FL, da Silva MCP, Marcon J, Dias ACF, de Mela IS, de Souza AP, Andreote FD, de Oliveira VM (2017) Functional metagenomics of oil-impacted mangrove sediments reveals high abundance of hydrolases of biotechnological interest. World J Microbiol Biotechnol 33:141CrossRefGoogle Scholar
  41. Pan Y, Chen J, Zhou H, Farzana S, Tam NFY (2017) Vertical distribution of dehalogenating bacteria in mangrove sediment and their potential to remove polybrominated diphenyl ether contamination. Mar Poll Bull 124:1055–1062CrossRefGoogle Scholar
  42. Panda M, Murthy TVR, Samal RN, Lele N, Patnaik AK, Chand PK (2017) Diversity of true and mangrove associates of Bhitarkanika national park (Odisha), India. Int J Adv Res 5:1784–1798Google Scholar
  43. Peixoto R, Chaer GM, Carmo FL, Araújo FV, Paes JE, Volpon A, Santiago GA, Rosado AS (2011) Bacterial communities reflect the spatial variation in pollutant levels in Brazilian mangrove sediment. Antonie van Leeuwenhoek 99:341–354CrossRefGoogle Scholar
  44. Pires ACC, Cleary DFR, Almeida A, Cunha A, Dealtry S, Mendonça-Hagler LCS, Smalla K, Gomes NCM (2012) Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Appl Environ Microbiol 78:5520–5528CrossRefGoogle Scholar
  45. Quero GM, Cassin D, Botter M, Perini L, Luna GM (2015) Patterns of benthic bacterial diversity in coastal areas contaminated by heavy metals, polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs). Front Microbiol 6:1053CrossRefGoogle Scholar
  46. Reef R, Feller IC, Lovelock CE (2010) Invited review: part of an invited issue on tree nutrition: nutrition of mangroves. Tree Physiol. 30:1148–1160CrossRefGoogle Scholar
  47. Rocha LL, Colares GB, Nogueira VLR, Paes FA, Melo VMM (2016) Distinct habitats select particular bacterial communities in mangrove sediments. Int J Micobiol 2016:3435809Google Scholar
  48. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Horn DJV, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  49. Tam NFY, Wong YS (1993) Retention of nutrients and heavy metals in mangrove sediment receiving wastewater of different strengths. Environ Technol 8:719–729CrossRefGoogle Scholar
  50. Thatoi H, Behera BC, Dangar TK, Mishra RR (2012) Microbial biodiversity in mangrove soils of Bhitarkanika, Odisha, India. Int J Environ Biol 2:50–58Google Scholar
  51. Upadhyay VP, Mishra PK (2010) Phenology of mangroves tree species on Orissa coast India. Trop Ecol 51:289–295Google Scholar
  52. Upadhyay VP, Mishra PK (2014) An ecological analysis of mangroves ecosystem of Odisha on the eastern coast of India. Proc Indian Nat Sci Acad 80:647–661CrossRefGoogle Scholar
  53. Uroz S, Ioannidis P, Lengelle J, Cébron A, Morin E, Buée M, Martin F (2013) Functional assays and metagenomic analyses reveals differences between the microbial communities inhabiting the soil horizons of a Norway spruce plantation. PLoS One 8:e55929CrossRefGoogle Scholar
  54. Varon-Lopez M, Dias ACF, Fasanella CC, Durrer A, Melo IS, Kuramae EE, Andreote FD (2014) Sulphur-oxidising and sulphate-reducing communities in Brazilian mangrove sediments. Environ Microbiol 16:845–855CrossRefGoogle Scholar
  55. Wang G, Meng K, Luo H, Wang Y, Huang H, Shi P, Yang P, Zhang Z, Yao B (2012) Phylogenetic diversity and environment-specific distributions of glycosyl hydrolase family 10 xylanases in geographically distant soils. PLoS One 7:e43480CrossRefGoogle Scholar
  56. Widdel F, Knittel K, Galushko A (2010) Handbook of hydrocarbon and lipid microbiology. Timmis KN, editor. Germany: Springer-Verlag Berlin Heidelberg; 2010. Anaerobic hydrocarbon-degrading microorganisms: an overview; pp. 1997–2022Google Scholar
  57. Wu P, Xiong X, Xu Z, Lu C, Cheng H, Zhang J, He W, Deng W, Lyu Y, Lou Q, Fang H (2016) Bacterial communities in the rhizospheres of three mangrove tree species from Beilun estuary, China. PLoS One 11:e0164082CrossRefGoogle Scholar
  58. Yang J, Ma L, Jiang H, Wu G, Dong H (2016) Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan lakes. Sci Rep 6:25078CrossRefGoogle Scholar
  59. Zhang Y, Dong J, Yang Z, Zhang S, Wang Y (2008) Phylogenetic diversity of nitrogen-fixing bacteria in mangrove sediments assessed by PCR–denaturing gradient gel electrophoresis. Arch. Microbiol. 190:19–28CrossRefGoogle Scholar
  60. Zhou C, Assem M, Tay JC, Watkins PB, Blumberg B, Schuetz EG, Thummel KE (2006) Steroid and xenobiotic receptor and vitamin D receptor crosstalk mediates CYP24 expression and drug-induced osteomalacia. J Clin Invest 116:1703–1712CrossRefGoogle Scholar
  61. Zhu H, Wang Y, Wang X, Luan T, Tam NFY (2014) Distribution and accumulation of polybrominated diphenyl ethers (PBDEs) in Hong Kong mangrove sediments. Sci Total Environ 468:130CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Pratiksha Behera
    • 1
  • Madhusmita Mohapatra
    • 1
  • Ji Yoon Kim
    • 2
  • Tapan K. Adhya
    • 3
  • Ajit K. Pattnaik
    • 1
  • Gurdeep Rastogi
    • 1
    Email author
  1. 1.Wetland Research and Training CentreChilika Development AuthorityBalugaonIndia
  2. 2.Department of Integrated Biological SciencePusan National UniversityBusanSouth Korea
  3. 3.School of BiotechnologyKIIT UniversityBhubaneswarIndia

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