Abstract
Microarthropods are known as vectors for soil microorganisms, predominantly fungi. This laboratory study uses the widespread unicellular green algae Chlorella vulgaris as model to assess the role of Collembola in algal dispersal and to determine the effects of gut passage on propagation. Living algal cells were observed in 70 % of the faecal pellets of Folsomia candida, Heteromurus nitidus and Protaphorura fimata. Moreover, marker fatty acids for green algae, i.e. 16:2ω6,9 and 16:3ω3,6,9, were consistently detected in the pellets. Compared to the algal diet, the high content of methyl-branched total lipid fatty acid (TLFA) with hydroxyl substitution indicated microbial colonisation during gut passage. The TLFA profile of faeces revealed no species-specific differences but similar changes in microbial communities over the duration of feeding, indicating comparable indigenous bacteria and colonisation mechanisms during gut passage. In sum, faecal pellets of soil microarthropods such as Collembola can act as a vector for both dietary algae and specific gut-associated microorganisms, with the latter likely involved in resource degradation inside and outside the gut habitat.
References
Borkott H, Insam H (1990) Symbiosis with bacteria enhances the use of chitin by springtail, Folsomia candida (Collembola). Biol Fertil Soils 9:126–129
Broday PA (1979) Feeding studies on the collembolan Cryptopygus antarcticus Willem at Signy Island, South Orkney Island. Brit Antarct Surv B 48:37–46
Buse T, Ruess L, Filser J (2013) New trophic biomarker for Collembola reared on algal diets. Pedobiologia 56:153–159
Christiansen K (1964) Bionomics of Collembola. Annu Rev Entomol 9:147–178
Davidson MM, Broday PA (1996) Analysis of cut contents of Gomphiocephalus hodgsoni Carpenter (Collembola: Hypogastruidae) at Cape geology, Antarctica. Polar Biol 16:463–467
Dromph KM (2001) Dispersal of entomopathogenic fungi by collembolans. Soil Biol Biochem 33:2047–2051
Dungait JAJ, Briones MJI, Bol R, Evershed RP (2008) Enhancing the understanding of earthworm feeding behaviour via the use of fatty acid δ13C values determined by gas chromatography-combustion-isotope ratio mass spectrometry. Rapid Commun Mass Sp 22:1643–1652
Fountain MT, Hopkin SP (2005) Folsomia candida (Collembola): a standard soil arthropod. Annu Rev Entomol 50:201–222
Gómez-Brandón M, Aira M, Lores M, Dominguez J (2011) Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes. PLoS One 6:e24786. doi:10.1371/journal.pone.0024786
Hubert J, Lukešová A (2001) Feeding of panphytophagous oribatid mite Scheloribates laevigatus (Acari: Oribatida) on cyanobacterial and algal diets in laboratory experiments. Appl Soil Ecol 16:77–83
Hunt ME, Floyed GL, Stout BB (1979) Soil algae in field and forest environments. Ecology 60:362–375
Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function and taxonomic significance. Microbiol Rev 55:288–302
Knapp BA, Podmirseg SM, Seeber J, Meyer E, Insam H (2009) Diet-related composition of the gut microbiota of Lumbricus rubellus as revealed by a molecular fingerprinting technique and cloning. Soil Biol Biochem 41:2299–2307
Lilleskov EA, Bruns TD (2005) Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97:762–769
Meier FA, Scherrer S, Honegger R (2002) Faecal pellets of lichenivorous mites contain viable cells of the lichen-forming ascomycete Xanthoria parietina and its green algal photobiont, Trebouxia arboricola. Biol J Linn Soc 76:259–268
Metting B (1981) The systematics and ecology of soil algae. Bot Rev 47:195–312
Rindi F, Allali HA, Lam DW, López-Bautista JM (2011) An overview of the biodiversity and biogeography of terrestrial green algae. In: Rescigno V, Maletta S (eds) Biodiversity hotspots. Nova Science Publishers Inc., New York, pp 105–122
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/
Ruess L, Chamberlain PM (2010) The fat that matters: soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biol Biochem 42:1898–1910
Ruess L, Schütz K, Haubert D, Häggblom MM, Kandeler E, Scheu S (2005) Application of lipid analysis to understand trophic interactions in soil. Ecology 86:2075–2082
Ruess L, Schütz K, Migge-Kleian S, Häggblom MM, Kandeler E, Scheu S (2007) Lipid composition of Collembola and their food resources in deciduous forest stands: implications for feeding strategies. Soil Biol Biochem 39:1990–2000
Scheu S, Folger M (2004) Single and mixed diets in Collembola: effects on reproduction and stable isotope fractionation. Funct Ecol 18:94–102
Stefaniak O, Seniczak S (1981) The effect of fungal diet on the development of Oppia nitens (Acri, Orbatei) and on the microflora of its alimentary tract. Pedobiologia 21:202–210
Stromberger ME, Keith AM, Schmidt O (2012) Distinct microbial and faunal communities and translocated carbon in Lumbricus terrestris drilopshere. Soil Biol Biochem 46:155–162
Tebbe CC, Czarnetzki AB, Thimm T (2006) Collembola as a habitat for microorganisms. In: König H, Varma A (eds) Soil biology, vol 6., Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 133–153
Thimm T, Hoffmann A, Borkott H, Munch JC, Tebbe CC (1998) The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but selective habitat and vector for microorganisms. Appl Environ Microb 64:2660–2669
Tiunov AV, Scheu S (2005) Arbuscular Mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 142:636–642
Vegter JJ (1983) Food and habitat specialization in coexisting springtails (Collembola, Entomobryidae). Pedobiologia 25:253–262
Verhoef HA, Prast JE, Verweij RA (1988) Relative importance of fungi and algae in the diet and nitrogen nutrition of Orchisella cincta (L.) and Tomocerus minor (Lubbock) (Collembola). Funct Ecol 2:195–201
Visser S (1985) Role of soil invertebrates in determining the composition of soil microbial communities. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecology interactions in soil. Blackwell Scientific Publications, Oxford, pp 297–317
Williams RH, Whipps JM, Cooke RC (1998) Role of soil mesofauna in dispersal of Coniothyrium minitans: mechanisms of transmission. Soil Biol Biochem 30:1937–1945
Wolf MM, Rockett CL (1984) Habitat changes affecting bacterial composition in the alimentary canal of oribatid mites (Acari: Oribatida). Int J Acarol 10:209–215
Wolters W (1985) Resource allocation in Tomocerus flavescens (Insecta, Collembola): a study with C-14-labelled food. Oecologia 65:229–235
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccarides in the characterization of microbial communities in soil: a review. Biol Fert Soils 29:111–129
Acknowledgments
We thank W. Wosnoik for his helpful comments in statistical analysing, P. Heese for her excellent technical assistance, R. Nehring for his much-appreciated help with fatty acid analysis by GC-mass spectrometry and J. Seeger for linguistic correction.
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Buse, T., Ruess, L. & Filser, J. Collembola gut passage shapes microbial communities in faecal pellets but not viability of dietary algal cells. Chemoecology 24, 79–84 (2014). https://doi.org/10.1007/s00049-013-0145-y
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DOI: https://doi.org/10.1007/s00049-013-0145-y