Skip to main content

Advertisement

Log in

Ex-situ enzyme activity and bacterial community diversity through soil depth profiles in penguin and seal colonies on Vestfold Hills, East Antarctica

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The soils impacted by sea animal excreta are important sources of nutrients in Antarctic terrestrial ecosystems, and soil microorganisms are the principal drivers of carbon and nitrogen cycling. However, microbial diversity and enzyme activities in these soils have still received little attention. In this paper, we investigated the distribution characteristics of bacterial community in four penguin and seal colony soil profiles collected in East Antarctica, using 16S rDNA-DGGE and real-time quantitative PCR. Soil microbial biomass carbon (Cmic), soil respiration (SR), and enzyme activities involved in carbon, nitrogen, and phosphorus metabolisms were also measured. Overall soil Cmic, SR, enzyme activities, and bacterial abundance decreased with depth. The bacterial abundance had a significant correlation with soil organic carbon and total nitrogen and highly corresponded to the relative content of penguin guano or seal excreta in these soil profiles. The 16S rDNA-DGGE revealed the complicated bacterial community structure in penguin and seal colony soils, and the band richness and dominant bands decreased with soil depth. Cluster analysis of DGGE profiles indicated that bacterial community in those soil profiles were divided into four main categories with the bacterial genetic similarity of 22 %, and the majority of the sequenced bands were Proteobacteria (α, β, γ), Actinobacteria, Bacteroidetes, Deinococcus-Thermus, Chloroflexi, and Firmicutes. Our results indicated that the deposition of penguin guano or seal excreta, which caused the variability in soil soil organic carbon, total nitrogen, pH, and soil moisture, might have an important effect on the vertical distribution pattern of bacterial abundance and diversity in Antarctic soil profiles.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aislabie JM, Chhour K, Saul DJ, Miyauchi S, Ayton J, Paetzold RF, Balks MR (2006) Dominant bacteria in soils of Marble Point and Wright Valley, Victoria Land, Antarctica. Soil Biol Biochem 38:3041–3056

    Article  CAS  Google Scholar 

  • Aislabie JM, Jordan S, Barker GM (2008) Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144:9–20

    Article  CAS  Google Scholar 

  • Aislabie JM, Jordan S, Ayton JL, Klassen GM (2009) Bacterial diversity associated with ornithogenic soil of the Ross Sea region, Antarctica. Can J Microbiol 55:21–36

    Article  PubMed  CAS  Google Scholar 

  • Beyer L, Knicker H, Blume H-P, Bölter M, Vogt B, Schneider D (1997) Soil organic matter of suggested spodic horizons in relic ornithogenic soils of coastal continental Antarctica (Casey Station, Wilkes Land) in comparison with that of spodic soil horizons in Germany. Soil Sci 162:518–527

    Article  CAS  Google Scholar 

  • Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. PNAS 105:10583–10588

    Article  PubMed  CAS  Google Scholar 

  • Bokhorst S, Huiskes AHL, Convey P, Van Bodegom PM, Aerts R (2008) Climate change effects on soil arthropod communities from the Falkland Islands and the Maritime Antarctic. Soil Biol Biochem 40:1547–1556

    Article  CAS  Google Scholar 

  • Bölter M (1989) Microbial activity in soils from Antarctica (Casey Station, Wilkes Land). Proc NIPR Symp Polar Biol 2:146–153

    Google Scholar 

  • Bölter M (1992) Environmental conditions and microbial properties from soils and lichens from Antarctica (Casey Station, Wilkes Land). Polar Biol 11:591–599

    Article  Google Scholar 

  • Bölter M, Blume HP, Schneider D, Beyer L (1997) Soil properties and distributions of invertebrates and bacteria from King George Island (Arctowski Station), Maritime Antarctic. Polar Biol 18:295–304

    Article  Google Scholar 

  • Bölter M, Kandeler E, Pietr SJ, Seppelt RD (2002) Heterotrophic soil microbes, microbial and enzymatic activity in antarctic soils. In: Beyer L, Bölter M (eds) Geoecology of Antarctic ice-free coastal landscapes. Ecological studies, vol 154. Springer, Berlin, pp 189–208

    Chapter  Google Scholar 

  • Brinkmann M, Pearce DA, Convey P, Ott S (2007) The cyanobacterial community of polygon soils at an inland Antarctic nunatak. Polar Biol 30:1505–1511

    Article  Google Scholar 

  • Cary SC, McDonld IR, Barrent JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8:129–138

    Article  PubMed  CAS  Google Scholar 

  • Chong CW, Annie TGY, Richard CS (2009a) DGGE fingerprinting of bacteria in soils from eight ecologically different sites around Casey Station, Antarctica. Polar Biol 32:853–860

    Article  Google Scholar 

  • Chong CW, Dunn MJ, Convey P (2009b) Environment influences on bacterial diversity of soils on Signy Island, maritime Antarctic. Polar Biol 32:1571–1582

    Article  Google Scholar 

  • Chong CW, Convey P, Pearce DA, Tan IKP (2012) Assessment of soil bacterial communities on Alexander Island (in the maritime and continental Antarctic transitional zone). Polar Biol 35:387–399

    Article  Google Scholar 

  • Chu HY, Neufeld JD, Walker VK, Grogan P (2011) The influence of vegetation type on soil bacterial, archaeal and fungal community structures in a low arctic tundra landscape. SSSAJ 75:1756–1765

    Article  CAS  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. PNAS 103:626–631

    Article  PubMed  CAS  Google Scholar 

  • Gordon DA, Priscu J, Giovannoni SJ (2000) Origin and phylogeny of microbes living in permanent Antarctic lake ice. Microb Ecol 39:197–202

    PubMed  Google Scholar 

  • Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2003) Influence of depth and sampling time on bacterial community structure in an upland grassland soil. FEMS Microbiol Ecol 43:35–43

    Article  PubMed  CAS  Google Scholar 

  • Guan YS (1986) Soil enzyme and its research methods. Agriculture Press, Beijing

    Google Scholar 

  • Hansel CM, Fendorf S, Jardine PM, Francis CA (2008) Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol 74:1620–1633

    Article  PubMed  CAS  Google Scholar 

  • Hofstee EH, Balks MR, Petchey F, Campbell DI (2006) Soils of Seabee Hook, Cape Hallett, northern Victoria Land, Antarctica. Antarct Sci 18:473–486

    Article  Google Scholar 

  • Hopkins DW, Sparrow AD, Shillam LL (2008) Enzymatic activities and microbial communities in an Antarctic dry valley soil: responses to C and N supplementation. Soil Biol Biochem 9:2130–2136

    Article  Google Scholar 

  • Huang T (2010) Holocene ecological responses of penguins and seals to the changes of Antarctic climate. University of Science and Technology of China, Hefei, pp 1–155

    Google Scholar 

  • Huang T, Sun LG, Wang YH, Zhu RB (2009) Penguin occupation in the Vestfold Hills. Antarct Sci 21:131–134

    Article  Google Scholar 

  • Huang J, Sun LG, Huang W, Wang XM (2010) The ecosystem evolution of penguin colonies in the past 8,500 years on Vestfold Hills, East Antarctica. Polar Biol 33:1399–1406

    Article  Google Scholar 

  • Isermeyer H (1952) Eine einfache Methode zur Bestimmung der Bodenatmung und der Karbonate im Boden. Zietschrift fur Pflanzenernahrung Bodenkunde 56:26–38

    Article  CAS  Google Scholar 

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  PubMed  CAS  Google Scholar 

  • Knox GA (1994) The biology of the Southern Ocean. Cambridge University Press, New York

    Google Scholar 

  • Lawley B, Ripley S, Bridge P, Convey P (2004) Molecular analysis of geographic patterns of eukaryotic diversity in Antarctic soils. Appl Environ Microbiol 70:5963–5972

    Article  PubMed  CAS  Google Scholar 

  • Li S, Xiao X, Yin X, Wang F (2006) Bacterial community along a historic lake sediment core of Ardley Island, west Antarctica. Extremophiles 10:461–467

    Article  PubMed  CAS  Google Scholar 

  • Lindeboom HJ (1984) The nitrogen pathway in a penguin rockery. Ecology 65:269–277

    Article  CAS  Google Scholar 

  • Lu J, Domingo JWS, Lamendella R, Edge T (2008) Phylogenetic diversity and molecular detection of bacterial in gull faces. Appl Environ Mcrobiol 74:3969–3976

    Article  CAS  Google Scholar 

  • Montague TL (1988) Birds of Prydz Bay, Antarctica: distribution and abundance. Hydrobiology 165:227–237

    Article  Google Scholar 

  • Moosvi SA, McDonald IR, Pearce DA (2005) Molecular detection and isolation from Antarctica of methylotrophic bacteria able to grow with methylated sulfur compounds. Syst Appl Microbiol 28:541–554

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Pearce DA, Vander Gast CJ, Lawley B (2003) Bacterioplankton community diversity in a maritime Antarctic lake, determined by culture-dependent and culture-independent techniques. FEMS Microbiol Ecol 45:59–70

    Article  PubMed  CAS  Google Scholar 

  • Peck LS, Clark MS, Clarke A (2005) Genomics: applications to Antarctic ecosystems. Polar Biol 28:351–365

    Article  Google Scholar 

  • Ravenschlag K, Sahm K, Pernthaler J, Amann R (1999) High bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65:3982–3989

    PubMed  CAS  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  • Sanyika TW, Stafford W, Cowan DA (2012) The soil and plant determinants of community structures of the dominant actinobacteria in Marion Island terrestrial habitats, Sub-Antarctica. Polar Biol 35:1129–1141

    Article  Google Scholar 

  • Seppelt RD, Broady PA, Pickard J, Adamson DA (1988) Plants and landscape in the Vestfold Hills, Antarctica. Hydrobiologia 165:185–196

    Article  Google Scholar 

  • Shivaji S, Reddy GS, Aduri RP, Kutty R, Ravenschlag K (2004) Bacterial diversity of a soil sample from Schirmacher Oasis, Antarctica. Cell Mol Biol 50:525–536

    PubMed  CAS  Google Scholar 

  • Simas FNB, Schaefer CEGR, Melo VF, Albuquerque-Filho MR, Michel RFM, Pereira VV, Gomes MRM, da Costa LM (2007) Ornithogenic cryosols from maritime Antarctica: phosphatization as a soil forming process. Geoderma 138:191–203

    Article  CAS  Google Scholar 

  • Speir TW, Cowling JC (1984) Ornithogenic Soils of the Cape Bird Adelie Penguin Rookeries, Antarctica. 1. Chemical properties. Polar Biol 2:199–205

    Article  Google Scholar 

  • Speir TW, Ross DJ (1984) Ornithogenic soils of the Cape Bird Adelie Penguin rookeries, Antarctica. 2. Ammonia evolution and enzyme activities. Polar Biol 2:207–212

    Article  Google Scholar 

  • Stephen JR, McCaig AE, Smith Z, Prosser JI (1996) Molecular diversity of soil and marine 16S rRNA gene sequences related to β-subgroup ammonia-oxidizing bacteria. Appl Environ Microbiol 62:4147–4157

    PubMed  CAS  Google Scholar 

  • Stomeo F, Makhalanyane TP, Valverde A, Pointing SB, Stevens MI, Cary CS, Tuffin MI, Cowan DA (2012) Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated Antarctic Dry Valley. FEMS Microbiol Ecol 82:326–340

    Article  PubMed  CAS  Google Scholar 

  • Sun LG, Xie ZQ, Zhao JL (2000) A 3,000-year record of penguin populations. Nature 407:858

    Article  PubMed  CAS  Google Scholar 

  • Tatur A (2002) Ornithogenic ecosystems in the maritime Antarctic–formation, development and disintegration. In: Beyer L, Bölter M (eds) Geoecology of Antarctic ice-free coastal landscapes. Ecological studies, vol 154. Springer, Berlin, pp 161–181

    Chapter  Google Scholar 

  • Tatur A, Myrcha A, Niegodzisz J (1997) Formation of abandoned penguin rookery ecosystems in the maritime Antarctic. Polar Biol 17:405–417

    Article  Google Scholar 

  • Teixeira LC, Peixoto RS, Cury JC (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J 4:989–1001

    Article  PubMed  Google Scholar 

  • Tring SG, Von MC, Kobayashi A, Salamov AA, Chen K, Chang HW et al (2005) Comparative metagenomics of microbial communities. Science 308:554–557

    Article  Google Scholar 

  • Ugolini FC (1972) Ornithogenic soils of Antarctica. Antarct Res Ser 20:181–193

    Article  CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Vishniac HS (1993) The microbiology of Antarctic soils. In: Friedmann EI (ed) Antarctic microbiology. Wiley-Liss, New York, pp 279–341

    Google Scholar 

  • Wu YC, Lu L, Wang BZ, Lin XG, Jia ZJ (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. SSSAJ 75:1431–1439

    Article  CAS  Google Scholar 

  • Xiao X, Yin X, Lin J (2005) Chitinase genes in lake sediments of Ardley Island, Antarctica. Appl Environ Microbial 71:7904–7909

    Article  CAS  Google Scholar 

  • Yergeau E, Kowalchuk GA (2008) Responses of Antarctic soil microbial communities and associated functions to temperature and freeze–thaw cycle frequency. Environ Microbiol 10:2223–2235

    Article  PubMed  Google Scholar 

  • Yergeau E, Bokhorst S, Huiskes AHL, Boschker HTS, Aerts R, Kowalchuk GA (2007a) Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiol Ecol 59:436–451

    Article  PubMed  CAS  Google Scholar 

  • Yergeau E, Kang S, He Z, Zhou J, Kowalchuk GA (2007b) Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J 1:163–179

    Article  PubMed  CAS  Google Scholar 

  • Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007c) Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ Microbiol 9:2670–2682

    Article  PubMed  CAS  Google Scholar 

  • Zdanowski MK, Veglenski P, Golik P (2004) Bacterial diversity in Adelie penguin, pygoscelis adeliae, guano: molecular and morpho-physiological approaches. FEMS Microbiol Ecol 50:163–173

    Article  PubMed  CAS  Google Scholar 

  • Zdanowski MK, Zmuda MJ, Zwolska I (2005) Bacterial role in the decomposition of marine-derived material (penguin guano) in the terrestrial maritime Antarctic. Soil Biol Biochem 37:581–592

    Article  CAS  Google Scholar 

  • Zhou LK (1987) Soil enzymology. Science Press, Beijing

    Google Scholar 

  • Zhou J, Xia B, Huang H, Treves DS, Wu LY, Marsh TL (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68:326–334

    Article  PubMed  CAS  Google Scholar 

  • Zhu RB, Sun JJ, Liu YS (2011) Potential ammonia emissions from penguin guano, ornithogenic soils and seal colony soils in coastal Antarctica: effects of freezing-thawing cycles and selected environmental variables. Antarct Sci 23:78–92

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 41076124; 41176171), Specialized Research Fund for the Doctoral Program of Higher Education (Grant No. 20123402110026) and the Fundamental Research Funds for the Central Universities (Grant No. WK2060190007). We thanked Y. Q. Liang, H. Sun, and Y. Feng for laboratory assistance and experimental guidance. We sincerely acknowledged the members of the 22nd Chinese National Antarctic Research Expedition for assistance with sample collection. We are also grateful to the anonymous reviewers and editor for their helpful revision and comments on a previous version of this paper.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Renbin Zhu or Haiyan Chu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 46 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ma, D., Zhu, R., Ding, W. et al. Ex-situ enzyme activity and bacterial community diversity through soil depth profiles in penguin and seal colonies on Vestfold Hills, East Antarctica. Polar Biol 36, 1347–1361 (2013). https://doi.org/10.1007/s00300-013-1355-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-013-1355-z

Keywords

Navigation