Advertisement

Mangrove Sediment Microbiome: Adaptive Microbial Assemblages and Their Routed Biogeochemical Processes in Yunxiao Mangrove National Nature Reserve, China

  • Xiaolan Lin
  • Buce Hetharua
  • Lian Lin
  • Hong Xu
  • Tianling Zheng
  • Zhili He
  • Yun Tian
Environmental Microbiology

Abstract

Microorganisms play important roles in mangrove ecosystems. However, we know little about the ecological implications of mangrove microbiomes for high productivity and the efficient circulation of elements in mangrove ecosystems. Here, we focused on mangrove sediments located at the Yunxiao National Mangrove Reserve in southeast China, uncovering the mangrove microbiome using the 16S rRNA gene and shotgun metagenome sequencing approaches. Physicochemical assays characterized the Yunxiao mangrove sediments as carbon (C)-rich, sulfur (S)-rich, and nitrogen (N)-limited environment. Then phylogenetic analysis profiling a distinctive microbiome with an unexpected high frequency of Chloroflexi and Nitrospirae appeared to be an adaptive characteristic of microbial structure in S-rich habitat. Metagenome sequencing analysis revealed that the metabolic pathways of N and S cycling at the community-level were routed through ammonification and dissimilatory nitrate reduction to ammonium for N conservation in this N-limited habitat, and dissimilatory sulfate reduction along with polysulfide formation for generating bioavailable S resource avoiding the biotoxicity of sulfide in mangrove sediments. In addition, methane metabolism acted as a bridge to connect C cycling to N and S cycling. Further identification of possible biogeochemical linkers suggested Syntrophobacter, Sulfurovum, Nitrospira, and Anaerolinea potentially drive the coupling of C, N, and S cycling. These results highlighting the adaptive routed metabolism flow, a previously undescribed property of mangrove sediment microbiome, appears to be a defining characteristic of this habitat and may significantly contribute to the high productivity of mangrove ecosystems, which could be used as indicators for the health and biodiversity of mangrove ecosystems.

Keywords

Mangrove ecosystem Mangrove sediment microbiome Biogeochemical processes High productivity Element circulation 

Notes

Acknowledgments

We would like to thank Professor John Hodgkiss of the City University of Hong Kong for correcting the English in this manuscript.

Funding

This work was financially supported by the National Key Research and Development Program of China (2017YFC05061001).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Supplementary material

248_2018_1261_MOESM1_ESM.pdf (163 kb)
ESM 1 (PDF 162 kb)

References

  1. 1.
    Barbier EB, Koch EW, Silliman BR, Hacker SD, Wolanski E, Primavera J, Granek EF, Polasky S, Aswani S, Cramer LA (2008) Coastal ecosystem-based management with nonlinear ecological functions and values. Science 319:321–323CrossRefGoogle Scholar
  2. 2.
    Pijush B, Arnab P, Sohan S, Sudip N, Anish B, Debojyoti R, Rudradip P, Abhrajyoti G, Dhrubajyoti C, Maitree B (2016) Bacterial diversity assessment of pristine mangrove microbial community from Dhulibhashani, Sundarbans using 16S rRNA gene tag sequencing. Genom Data 7:76–78CrossRefGoogle Scholar
  3. 3.
    Gomes NCM, Flocco CG, Costa R, Junca H, Vilchez R, Pieper DH, Krögerrecklenfort E, Paranhos R, Mendonçahagler 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
  4. 4.
    Alongi DM (1988) Bacterial productivity and microbial biomass in tropical mangrove sediments. Microb Ecol 15:59–79CrossRefGoogle Scholar
  5. 5.
    Zhou HW, Wong AHY, Yu RMK, Yongdoo P, Yukshan W, Tam NFY (2009) Polycyclic aromatic hydrocarbon-induced structural shift of bacterial communities in mangrove sediment. Microb Ecol 58:153–160CrossRefGoogle Scholar
  6. 6.
    Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Kent AD, Daroub SH, Camargo FA, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290CrossRefGoogle Scholar
  7. 7.
    Ligi T, Oopkaup K, Truu M, Preem JK, Nõlvak H, Mitsch WJ, Mander Ü, Truu J (2014) Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing. Ecol Eng 72:56–66CrossRefGoogle Scholar
  8. 8.
    Galand PE, Casamayor EO, Kirchman DL, Lovejoy C, Karl DM (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci U S A 106:22427–22432CrossRefGoogle Scholar
  9. 9.
    Zhu YG, Xue XM, Kappler A, Rosen BP, Meharg AA (2017) Linking genes to microbial biogeochemical cycling: lessons from arsenic. Environ Sci Technol 51:7326–7339CrossRefGoogle Scholar
  10. 10.
    Acf D, Andreote FD, Diniandreote F, Lacava PT, Alb S, Melo IS, Azevedo JL, Araújo WL (2009) Diversity and biotechnological potential of culturable bacteria from Brazilian mangrove sediment. World J Microbiol Biotechnol 25:1305–1311CrossRefGoogle Scholar
  11. 11.
    Dias ACF, Andreote FD, Rigonato J, Fiore MF, Melo IS, Araújo WL (2010) The bacterial diversity in a Brazilian non-disturbed mangrove sediment. Antonie Van Leeuwenhoek 98:541–551CrossRefGoogle Scholar
  12. 12.
    Andreote FD, Jiménez DJ, Chaves D, Dias ACF, Luvizotto DM, Dini-Andreote F, Fasanella CC, Lopez MV, Baena S, Taketani RG (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS One 7:e38600CrossRefGoogle Scholar
  13. 13.
    Chakraborty A, Bera A, Mukherjee A, Basak P, Khan I, Mondal A, Roy A, Bhattacharyya A, Sengupta S, Roy D (2015) Changing bacterial profile of Sundarbans, the world heritage mangrove: impact of anthropogenic interventions. World J Microbiol Biotechnol 31:593–610CrossRefGoogle Scholar
  14. 14.
    Basak P, Pramanik A, Roy R, Chattopadhyay D, Bhattacharyya M (2015) Cataloguing the bacterial diversity of the Sundarbans mangrove, India in the light of metagenomics. Genom Data 4:90–92CrossRefGoogle Scholar
  15. 15.
    Alzubaidy H, Essack M, Malas TB, Bokhari A, Motwalli O, Kamanu FK, Jamhor SA, Mokhtar NA, Antunes A, Simões MF (2016) Rhizosphere microbiome metagenomics of gray mangroves (Avicennia marina) in the Red Sea. Gene 576:626–636CrossRefGoogle Scholar
  16. 16.
    Feller IC, Lovelock CE, Berger U, Mckee KL, Joye SB, Ball MC (2010) Biocomplexity in mangrove ecosystems. Annu Rev Mar Sci 2:395–417CrossRefGoogle Scholar
  17. 17.
    Abhrajyoti G, Nirmalya D, Amit B, Amit T, Sathyaniranjan KB, Kalyan C, Dhrubajyoti C (2010) Culture independent molecular analysis of bacterial communities in the mangrove sediment of Sundarban, India. Saline Systems 6:1CrossRefGoogle Scholar
  18. 18.
    Basak P, Majumder NS, Nag S, Bhattacharyya A, Roy D, Chakraborty A, Sengupta S, Roy A, Mukherjee A, Pattanayak R (2015) Spatiotemporal analysis of bacterial diversity in sediments of Sundarbans using parallel 16S rRNA gene tag sequencing. Microb Ecol 69:500–511CrossRefGoogle Scholar
  19. 19.
    Bai S, Li J, Tian Y, Lin G, Zheng T, Li J, He Z, Nostrand V, Tian Y, Lin G (2013) GeoChip-based analysis of the functional gene diversity and metabolic potential of soil microbial communities of mangroves. Appl Microbiol Biotechnol 97:7035–7048CrossRefGoogle Scholar
  20. 20.
    Graham EB, Knelman JE, Schindlbacher A, Siciliano S, Breulmann M, Yannarell A, Beman JM, Abell G, Philippot L, Prosser J (2016) Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front Microbiol 7:214PubMedPubMedCentralGoogle Scholar
  21. 21.
    Abed RM, Alkindi S, Alkharusi S (2015) Diversity of bacterial communities along a petroleum contamination gradient in desert soils. Microb Ecol 69:95–105CrossRefGoogle Scholar
  22. 22.
    Bardgett RD, WHvd P (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511CrossRefGoogle Scholar
  23. 23.
    Prosser JI, Bohannan BJ, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, Green JL, Green LE, Killham K, Lennon JJ (2007) The role of ecological theory in microbial ecology. Nat Rev Microbiol 5:384–392CrossRefGoogle Scholar
  24. 24.
    Baker BJ, Lazar CS, Teske AP, Dick GJ (2015) Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome 3:14CrossRefGoogle Scholar
  25. 25.
    Holmer M, Kristensen E, Banta G, Hansen K, Jensen MH, Bussawarit N (1994) Biogeochemical cycling of sulfur and iron in sediments of a south-east Asian mangrove, Phuket Island, Thailand. Biogeochemistry 26:145–161CrossRefGoogle Scholar
  26. 26.
    Wang Q, George MG, James T, James RC (2007) Naïve Bayesian Classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefGoogle Scholar
  27. 27.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  28. 28.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590CrossRefGoogle Scholar
  29. 29.
    Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113CrossRefGoogle Scholar
  30. 30.
    Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19:926–936CrossRefGoogle Scholar
  31. 31.
    Langille MG, Zaneveld J, Caporaso JG, Mcdonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821CrossRefGoogle Scholar
  32. 32.
    Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 27:29–34Google Scholar
  33. 33.
    Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Qi P, Liu Y (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18CrossRefGoogle Scholar
  34. 34.
    Li W, Godzik A (2006) Cd-Hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659CrossRefGoogle Scholar
  35. 35.
    Buchfink B, Xie C, Huson D (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60CrossRefGoogle Scholar
  36. 36.
    Ghiglione JF, Murray AE (2012) Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc Natl Acad Sci U S A 109:17633–17638CrossRefGoogle Scholar
  37. 37.
    Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 359:320–325.  https://doi.org/10.1126/science.aap9516 CrossRefPubMedGoogle Scholar
  38. 38.
    Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9:403–413CrossRefGoogle Scholar
  39. 39.
    Fernández-Gómez B, Richter M, Schüler M, Pinhassi J, Acinas SG, González JM, Pedrósalió C (2013) Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7:1026–1037CrossRefGoogle Scholar
  40. 40.
    Biddle JF, Fitzgibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci U S A 105:10583–10588CrossRefGoogle Scholar
  41. 41.
    Sekiguchi Y, Yamada T, Hanada S, Ohashi A, Harada H, Kamagata Y (2003) Anaerolinea thermophila gen. nov., sp. nov. and Caldilinea aerophila gen. nov., sp. nov., novel filamentous thermophiles that represent a previously uncultured lineage of the domain Bacteria at the subphylum level. Int J Syst Evol Microbiol 53:1843CrossRefGoogle Scholar
  42. 42.
    Lücker S, DeLong EF (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci U S A 107:13479–13484CrossRefGoogle Scholar
  43. 43.
    Mussmann M, Ishii K, Rabus R, Amann R (2005) Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ Microbiol 7:405–418CrossRefGoogle Scholar
  44. 44.
    Campbell B, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468CrossRefGoogle Scholar
  45. 45.
    Bhatnagar S, Badger JH, Madupu R, Khouri HM, O'Connor EM, Robb FT, Ward NL, Eisen JA (2015) Genome sequence of the sulfate-reducing thermophilic bacterium Thermodesulfovibrio yellowstonii strain DSM 11347T (Phylum Nitrospirae). Genome Announc 3:e01489–e01414PubMedPubMedCentralGoogle Scholar
  46. 46.
    Wu ML, van Teeseling MC, Willems MJ, van Donselaar EG, Klingl A, Rachel R, Geerts WJ, Jetten MS, Strous M, Van NL (2012) Ultrastructure of the denitrifying methanotroph “Candidatus Methylomirabilis oxyfera,” a novel polygon-shaped bacterium. J Bacteriol 194:284–291CrossRefGoogle Scholar
  47. 47.
    Kostan J, Sjöblom B, Maixner F, Mlynek G, Furtmüller PG, Obinger C, Wagner M, Daims H, Djinovićcarugo K (2010) Structural and functional characterisation of the chlorite dismutase from the nitrite-oxidizing bacterium “Candidatus Nitrospira defluvii”: identification of a catalytically important amino acid residue. J Struct Biol 172:331–342CrossRefGoogle Scholar
  48. 48.
    Park SJ, Ghai R, Rodríguezvalera F, Jung MY, Kim JG, Rhee SK (2012) Draft genome sequence of the sulfur-oxidizing bacterium “Candidatus Sulfurovum sediminum” AR, which belongs to the Epsilonproteobacteria. J Bacteriol 194:4128–4129CrossRefGoogle Scholar
  49. 49.
    Worm P, Stams AJ, Cheng X, Plugge CM (2011) Growth- and substrate-dependent transcription of formate dehydrogenase and hydrogenase coding genes in Syntrophobacter fumaroxidans and Methanospirillum hungatei. Microbiology 157:280–289CrossRefGoogle Scholar
  50. 50.
    Miflin BJ, Habash DZ (2002) Carbon and nitrogen relationships and signalling. The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53:979–987CrossRefGoogle Scholar
  51. 51.
    Fernandes SO, Michotey VD, Guasco S, Bonin PC, Bharathi PA (2012) Denitrification prevails over anammox in tropical mangrove sediments (Goa, India). Mar Environ Res 74:9–19CrossRefGoogle Scholar
  52. 52.
    Gardner WS, An S, Brock D (2006) Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51:558–568CrossRefGoogle Scholar
  53. 53.
    Boto K, Wellington J (1983) Phosphorus and nitrogen nutritional status of a northern Australian mangrove forest. Mar Ecol Prog Ser 11:63–69CrossRefGoogle Scholar
  54. 54.
    Feller IC, Mckee KL, Whigham DF, O’Neill JP (2003) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175CrossRefGoogle Scholar
  55. 55.
    Fernandes SO, Bonin PC, Michotey VD, Garcia N, Lokabharathi PA (2012) Nitrogen-limited mangrove ecosystems conserve N through dissimilatory nitrate reduction to ammonium. Sci Rep 2:419CrossRefGoogle Scholar
  56. 56.
    Kristensen E (2007) Carbon balance in mangrove sediments: the driving processes and their controls. Greenhouse gas and carbon balances in mangrove coastal ecosystems, In: Tateda Y et al. (ed) Gendai Tosho, Kanagawa, pp 61–78Google Scholar
  57. 57.
    Takagi H, Ohtsu I (2017) L-Cysteine metabolism and fermentation in microorganisms. Adv Biochem Eng Biotechnol 159:129–151PubMedGoogle Scholar
  58. 58.
    Findlay AJ (2016) Microbial impact on polysulfide dynamics in the environment. FEMS Microbiol Lett 363:fnw103CrossRefGoogle Scholar
  59. 59.
    Hedderich R, Klimmek O, Kröger A, Dirmeier R, Keller M, Stetter KO (1998) Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol Rev 22:353–381CrossRefGoogle Scholar
  60. 60.
    Berg JS, Schwedt A, Kreutzmann AC, Kuypers MM, Milucka J (2014) Polysulfides as intermediates in the oxidation of sulfide to sulfate by Beggiatoa spp. Appl Environ Microbiol 80:629–636CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Xiaolan Lin
    • 1
  • Buce Hetharua
    • 1
  • Lian Lin
    • 1
  • Hong Xu
    • 1
  • Tianling Zheng
    • 1
    • 2
  • Zhili He
    • 3
  • Yun Tian
    • 1
  1. 1.Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, School of Life SciencesXiamen UniversityXiamenChina
  2. 2.State Key Laboratory of Marine Environmental SciencesXiamen UniversityXiamenChina
  3. 3.Environmental Microbiomics Research Center, School of Environmental Science and EngineeringSun Yat-Sen UniversityGuangzhouChina

Personalised recommendations