Skip to main content

Advertisement

Log in

Faunal Burrows Alter the Diversity, Abundance, and Structure of AOA, AOB, Anammox and n-Damo Communities in Coastal Mangrove Sediments

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

In the present work, the diversity, community structures, and abundances of aerobic ammonia-oxidizing archaea (AOA) and bacteria (AOB), anaerobic ammonium-oxidizing (anammox) bacteria, and denitrifying anaerobic methane oxidization (n-damo) bacteria were unraveled in the bioturbated areas of the coastal Mai Po mangrove sediments. Results indicated that the bioturbation by burrowing in mangrove sediments was associated with higher concentration of NH4 + but lower concentrations of both NO2 and NO3 , and increase in diversity and richness of both AOA and AOB, but relatively lower diversity and richness of n-damo bacteria. The phylotypes of anammox bacterial community were significantly increased while their phylogenetic lineages observed in the less bioturbated areas were also maintained. Infauna also showed a great impact on the composition of n-damo bacterial phylotypes and burrowing activity altered the n-damo community structure profoundly in the sampled areas. The communities of n-damo bacteria in the surrounding bulk sediments showed similar structures to marine n-damo communities, but those on the burrow wall and in the ambient surface layer had a freshwater pattern, which was different from previous findings in Mai Po wetland. On the other hand, the abundances of AOA, AOB, and n-damo bacteria were greatly stimulated on burrow walls while the abundance of anammox bacteria remained unchanged. Infaunal burrows and mangrove roots affected the relative abundance of AOA and AOB. The benthic infauna stimulated the abundances of AOA, AOB, anammox, and n-damo bacteria. Furthermore, NH4 + and NO2 were important environmental factors changing the structure of each group. The communities of anammox and n-damo bacteria in bioturbated areas showed a competitive relationship.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Connell JH (1978) Diversity in tropical rain forests and coral reefs—high diversity of trees and corals is maintained only in a non-equilibrium state. Science 199:1302–1310

    Article  CAS  PubMed  Google Scholar 

  2. Stief P (2013) Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10:7829–7846

    Article  Google Scholar 

  3. Satoh H, Nakamura Y, Okabe S (2007) Influences of infaunal burrows on the community structure and activity of ammonia-oxidizing bacteria in intertidal sediments. Appl. Environ. Microbiol. 73:1341–1348

    Article  CAS  PubMed  Google Scholar 

  4. Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar. Ecol. Prog. Ser. 446:285–302

    Article  Google Scholar 

  5. Thamdrup B (2012) New pathways and processes in the global nitrogen cycle. Annu Rev Ecol Evol S 43:407–428

    Article  Google Scholar 

  6. Laverock B, Smith CJ, Tait K, Osborn AM, Widdicombe S, Gilbert JA (2010) Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments. ISME J 4:1531–1544

    Article  PubMed  Google Scholar 

  7. Satoh H, Okabe S (2013) Spatial and temporal oxygen dynamics in macrofaunal burrows in sediments: a review of analytical tools and observational evidence. Microbes Environ. 28:166–179

    Article  PubMed  PubMed Central  Google Scholar 

  8. Devol AH (2015) Denitrification, anammox, and n2 production in marine sediments. Annu. Rev. Mar. Sci. 7:403–423. doi:10.1146/annurev-marine-010213-135040

    Article  Google Scholar 

  9. Laverock B, Kitidis V, Tait K, Gilbert JA, Osborn AM, Widdicombe S (2013) Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 368:20120441. doi:10.1098/rstb.2012.0441

    Article  CAS  Google Scholar 

  10. Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, op de Camp HJM, Jetten MSM, Strous M (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ. Microbiol. 10:3164–3173

    Article  CAS  PubMed  Google Scholar 

  11. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MS, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548. doi:10.1038/nature08883

    Article  CAS  PubMed  Google Scholar 

  12. Ettwig KF, van Alen T, van de Pas-Schoonen KT, Jetten MSM, Strous M (2009) Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl. Environ. Microbiol. 75:3656–3662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damste JSS, Op den Camp HJM, Jetten MSM, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921

    Article  CAS  PubMed  Google Scholar 

  14. Hu BL, Shen LD, Lian X, Zhu Q, Liu S, Huang Q, He ZF, Geng S, Cheng DQ, Lou LP, Xu XY, Zheng P, He YF (2014) Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proc. Natl. Acad. Sci. U. S. A. 111:4495–4500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Deutzmann JS, Stief P, Brandes J, Schink B (2014) Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake. Proc. Natl. Acad. Sci. U. S. A. 111:18273–18278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Yang J, Jiang HC, Wu G, Hou WG, Sun YJ, Lai ZP, Dong HL (2012) Co-occurrence of nitrite-dependent anaerobic methane oxidizing and anaerobic ammonia oxidizing bacteria in two Qinghai-Tibetan saline lakes. Front. Earth Sci. 6:383–391

    Article  CAS  Google Scholar 

  17. Shen L, Liu S, He Z, Lian X, Huang Q, He Y, Lou L, Xu X, Zheng P, Hu B (2015) Depth-specific distribution and importance of nitrite-dependent anaerobic ammonium and methane-oxidising bacteria in an urban wetland. Soil Bio Biochem 83:43–51

    Article  CAS  Google Scholar 

  18. Wang Y, Zhu G, Harhangi HR, Zhu B, Jetten MS, Yin C, Op den Camp HJ (2012) Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane oxidizing bacteria in a paddy soil. FEMS Microbiol. Lett. 336:79–88

    Article  CAS  PubMed  Google Scholar 

  19. Shen LD, Liu S, Huang Q, Lian X, He ZF, Geng S, Jin RC, He YF, Lou LP, Xu XY, Zheng P, Hu BL (2014) Evidence for the cooccurrence of nitrite-dependent anaerobic ammonium and methane oxidation processes in a flooded paddy field. Appl. Environ. Microbiol. 80:7611–7619

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wang YF, Feng YY, Ma XJ, Gu J-D (2013) Seasonal dynamics of ammonia/ammonium-oxidizing prokaryotes in oxic and anoxic wetland sediments of subtropical coastal mangrove. Appl. Microbiol. Biotechnol. 97:7919–7934

    Article  CAS  PubMed  Google Scholar 

  21. Li M, Cao HL, Hong YG, Gu J-D (2011) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl. Microbiol. Biotechnol. 89:1243–1254

    Article  CAS  PubMed  Google Scholar 

  22. Li M, Cao HL, Hong YG, Gu J-D (2011) Seasonal dynamics of anammox bacteria in estuarial sediment of the Mai Po Nature Reserve revealed by analyzing the 16S rRNA and hydrazine oxidoreductase (hzo) genes. Microbes Environ. 26:15–22

    Article  CAS  PubMed  Google Scholar 

  23. Li M, Cao HL, Hong YG, Gu JD (2013) Using the variation of anammox bacteria community structures as a bio-indicator for anthropogenic/terrestrial nitrogen inputs in the Pearl River Delta (PRD). Appl. Microbiol. Biotechnol. 97:9875–9883

    Article  CAS  PubMed  Google Scholar 

  24. Cao H, Hong Y, Li M, Gu J-D (2012) Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea. Appl. Microbiol. Biotechnol. 94:247–259. doi:10.1007/s00253-011-3636-1

    Article  CAS  PubMed  Google Scholar 

  25. Han P, Li M, Gu J-D (2013) Biases in community structures of ammonia/ammonium-oxidizing microorganisms caused by insufficient DNA extractions from Baijiang soil revealed by comparative analysis of coastal wetland sediment and rice paddy soil. Appl. Microbiol. Biotechnol. 97:8741–8756

    Article  CAS  PubMed  Google Scholar 

  26. Chen J, Zhou ZC, Gu JD (2015) Complex community of nitrite-dependent anaerobic methane oxidation bacteria in coastal sediments of the Mai Po wetland by PCR amplification of both 16S rRNA and pmoA genes. Appl. Microbiol. Biotechnol. 99:1463–1473

    Article  CAS  PubMed  Google Scholar 

  27. Lee SY, Leung V (1999) The brachyuran Fauna of the Mai Po Marshes Nature Reserve and Deep Bay. Hong Kong University Press, Hong Kong

    Google Scholar 

  28. AFCD_HK (2014) Hong Kong species, Hong Kong mangrove fauna. Agriculture, Fisheries and Conservation Department of Hong Kong web. http://www.afcd.gov.hk/english/conservation/hkbiodiversity/speciesgroup/speciesgroup_mangrove.html. Accessed 06 April 2015.

  29. Li M, Cao HL, Hong YG, Gu J-D (2011) Mangrove trees affect the community structure and distribution of anammox bacteria at an anthropogenic-polluted mangrove in the Pearl River Delta reflected by 16S rRNA and hydrazine oxidoreductase (HZO) encoding gene analyses. Ecotoxicology 20:1780–1790. doi:10.1007/s10646-011-0711-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wang YF, Gu J-D (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl. Microbiol. Biotechnol. 97:7015–7033

    Article  CAS  PubMed  Google Scholar 

  31. American Public Health Association (1995) Standard methods for the examination of water and wastewater, 19th edn. APHA, Washington D.C.

    Google Scholar 

  32. Wright ES, Yilmaz LS, Noguera DR (2012) DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl. Environ. Microbiol. 78:717–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hong YG, Li M, Cao HL, Gu JD (2011) Residence of habitat-specific anammox bacteria in the deep-sea subsurface sediments of the South China Sea: analyses of marker gene abundance with physical chemical parameters. Microb. Ecol. 62:36–47

    Article  PubMed  PubMed Central  Google Scholar 

  36. 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, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton, NJ, pp. 34–39

    Book  Google Scholar 

  38. Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand. J. Stat. 11:265–270

    Google Scholar 

  39. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27

    Article  CAS  PubMed  Google Scholar 

  40. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Paleontol Electro 4:9

    Google Scholar 

  41. Ter Braak CJF, Smilauer P (2002) CANOCO reference manual and user's guide to Canoco for windows: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca

    Google Scholar 

  42. Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546. doi:10.1038/nature03911

    Article  PubMed  Google Scholar 

  43. Chen J, Zhou ZC, Gu J-D (2014) Occurrence and diversity of nitrite-dependent anaerobic methane oxidation bacteria in the sediments of the South China Sea revealed by amplification of both 16S rRNA and pmoA genes. Appl. Microbiol. Biotechnol. 98:5685–5696

    Article  CAS  PubMed  Google Scholar 

  44. Luesken FA, van Alen TA, van der Biezen E, Frijters C, Toonen G, Kampman C, Hendrickx TL, Zeeman G, Temmink H, Strous M, Op den Camp HJ, Jetten MS (2011) Diversity and enrichment of nitrite-dependent anaerobic methane oxidizing bacteria from wastewater sludge. Appl. Microbiol. Biotechnol. 92:845–854. doi:10.1007/s00253-011-3361-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Luesken FA, Zhu BL, van Alen TA, Butler MK, Diaz MR, Song B, den Camp HJMO, Jetten MSM, Ettwig KF (2011) pmoA primers for detection of anaerobic methanotrophs. Appl. Environ. Microbiol. 77:3877–3880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Chen J, Jiang XW, Gu J-D (2015) Existence of novel phylotypes of nitrite-dependent anaerobic methane-oxidizing bacteria in surface and subsurface sediments of the South China Sea. Geomicrobiol J. 32:1–9

    Article  Google Scholar 

  47. Zhu G, Zhou L, Wang Y, Wang S, Guo J, Long XE, Sun X, Jiang B, Hou Q, Jetten MS, Yin C (2015) Biogeographical distribution of denitrifying anaerobic methane oxidizing bacteria in Chinese wetland ecosystems. Environ. Microbiol. Rep. 7:128–138. doi:10.1111/1758-2229.12214

    Article  CAS  PubMed  Google Scholar 

  48. Nizzoli D, Bartoli M, Cooper M, Welsh DT, Underwood GJC, Viaroli P (2007) Implications for oxygen, nutrient fluxes and denitrification rates during the early stage of sediment colonisation by the polychaete Nereis spp. in four estuaries. Estuar Coast Shelf S 75:125–134

    Article  Google Scholar 

  49. Lewandowski J, Laskov C, Hupfer M (2007) The relationship between Chironomus plumosus burrows and the spatial distribution of pore-water phosphate, iron and ammonium in lake sediments. Freshw. Biol. 52:331–343

    Article  CAS  Google Scholar 

  50. Stief P, Holker F (2006) Trait-mediated indirect effects of predatory fish on microbial mineralization in aquatic sediments. Ecology 87:3152–3159

    Article  PubMed  Google Scholar 

  51. Wang YF, Gu J-D (2014) Effects of allylthiourea, salinity, and pH on ammonia/ammonium-oxidizing prokaryotes in mangrove sediment incubated in laboratory microcosms. Appl. Microbiol. Biotechnol. 98:3257–3274

    Article  CAS  PubMed  Google Scholar 

  52. Ding XD, Fu L, Liu CJ, Chen FJ, Hoffland E, Shen JB, Zhang FS, Feng G (2011) Positive feedback between acidification and organic phosphate mineralization in the rhizosphere of maize (Zea mays L.). Plant Soil 349:13–24

    Article  CAS  Google Scholar 

  53. Lu HL, Yan CL, Liu JC (2007) Low-molecular-weight organic acids exuded by mangrove (Kandelia candel (L.) Druce) roots and their effect on cadmium species change in the rhizosphere. Environ. Exp. Bot. 61:159–166

    Article  CAS  Google Scholar 

  54. Shen LD, Liu S, Zhu Q, Li XY, Cai C, Cheng DQ, Lou LP, Xu XY, Zheng P, Hu BL (2014) Distribution and diversity of nitrite-dependent anaerobic methane-oxidising bacteria in the sediments of the qiantang river. Microb. Ecol. 67:341–349. doi:10.1007/s00248-013-0330-0

    Article  CAS  PubMed  Google Scholar 

  55. Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Medigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJM, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794

    Article  PubMed  Google Scholar 

  56. Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, den Camp HJMO, Harhangi HR, Janssen-Megens EM, Francoijs KJ, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M (2011) Molecular mechanism of anaerobic ammonium oxidation. Nature 479:127–U159

    Article  CAS  PubMed  Google Scholar 

  57. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan Z, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570. doi:10.1038/nature12375

    Article  CAS  PubMed  Google Scholar 

  58. Bernhard AE, Donn T, Giblin AE, Stahl DA (2005) Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ. Microbiol. 7:1289–1297

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This project was supported by Hong Kong PhD Fellowship (JC) and Hong Kong RGC GRF grant no. 701913 (J-DG). Additional financial support for this research project was from the laboratory fund. We thank Dr. Yong-Feng Wang for helping with the sampling, Dr. Kun Liu for assisting the real-time quantitative PCR and Ms. Kelly Lau for general laboratory assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ji-Dong Gu.

Electronic Supplementary Material

ESM 1

(DOC 2799 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, J., Gu, JD. Faunal Burrows Alter the Diversity, Abundance, and Structure of AOA, AOB, Anammox and n-Damo Communities in Coastal Mangrove Sediments. Microb Ecol 74, 140–156 (2017). https://doi.org/10.1007/s00248-017-0939-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-0939-5

Keywords

Navigation