Biological Soil Crusts from Different Soil Substrates Harbor Distinct Bacterial Groups with the Potential to Produce Exopolysaccharides and Lipopolysaccharides

Abstract

Biological soil crusts (biocrusts) play an important role in improving soil stability and resistance to erosion by promoting aggregation of soil particles. During initial development, biocrusts are dominated by bacteria. Some bacterial members of the biocrusts can contribute to the formation of soil aggregates by producing exopolysaccharides and lipopolysaccharides that act as “glue” for soil particles. However, little is known about the dynamics of “soil glue” producers during the initial development of biocrusts. We hypothesized that different types of initial biocrusts harbor distinct producers of adhesive polysaccharides. To investigate this, we performed a microcosm experiment, cultivating biocrusts on two soil substrates. High-throughput shotgun sequencing was used to obtain metagenomic information on microbiomes of bulk soils from the beginning of the experiment, and biocrusts sampled after 4 and 10 months of incubation. We discovered that the relative abundance of genes involved in the biosynthesis of exopolysaccharides and lipopolysaccharides increased in biocrusts compared with bulk soils. At the same time, communities of potential “soil glue” producers that were highly similar in bulk soils underwent differentiation once biocrusts started to develop. In the bulk soils, the investigated genes were harbored mainly by Betaproteobacteria, whereas in the biocrusts, the major potential producers of adhesive polysaccharides were, aside from Alphaproteobacteria, either Cyanobacteria or Chloroflexi and Acidobacteria. Overall, our results indicate that the potential to form exopolysaccharides and lipopolysaccharides is an important bacterial trait for initial biocrusts and is maintained despite the shifts in bacterial community composition during biocrust development.

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

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

References

  1. 1.

    Belnap J, Lange OL (2003) Biological soil crusts: structure, function, and management. Springer, New York

    Google Scholar 

  2. 2.

    Sancho LG, Maestre FT, Büdel B (2014) Biological soil crusts in a changing world: introduction to the special issue. Biodivers Conserv 23:1611–1617

    Google Scholar 

  3. 3.

    Wu Y, Rao B, Wu P, Liu Y, Li G, Li D (2013) Development of artificially induced biological soil crusts in fields and their effects on top soil. Plant Soil 370:115–124

    CAS  Google Scholar 

  4. 4.

    Rossi F, Mugnai G, De Philippis R (2018) Complex role of the polymeric matrix in biological soil crusts. Plant Soil 429:19–34

    CAS  Google Scholar 

  5. 5.

    Totsche KU, Amelung W, Gerzabek MH, Guggenberger G, Klumpp E, Knief C, Lehndorff E, Mikutta R, Peth S, Prechtel A (2018) Microaggregates in soils. J Plant Nutr Soil Sc 181:104–136

    CAS  Google Scholar 

  6. 6.

    Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics. Soil Till Res 79:7–31

    Google Scholar 

  7. 7.

    Abu-Lail NI, Camesano TA (2003) Role of lipopolysaccharides in the adhesion, retention, and transport of Escherichia coli JM109. Environ Sci Technol 37:2173–2183

    CAS  PubMed  Google Scholar 

  8. 8.

    Veste M, Littmann T, Breckle S-W, Yair A (2001) The role of biological soil crusts on desert sand dunes in the northwestern Negev, Israel. In: Breckle S-W, Veste M, Wucherer W (eds) Sustainable land use in deserts. Springer, Heidelberg, pp 357–367

    Google Scholar 

  9. 9.

    Selbmann L, Stingele F, Petruccioli M (2003) Exopolysaccharide production by filamentous fungi: the example of Botryosphaeria rhodina. Anton Leeuw Int J G 84:135–145

    CAS  Google Scholar 

  10. 10.

    Martínez-Cánovas MJ, Quesada E, Martínez-Checa F, del Moral A, Bejar V (2004) Salipiger mucescens gen. nov., sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium isolated from hypersaline soil, belonging to the α-proteobacteria. Int J Syst Evol Micr 54:1735–1740

    Google Scholar 

  11. 11.

    Suela Silva M, Naves Sales A, Teixeira Magalhães-Guedes K, Ribeiro Dias D, Schwan RF (2013) Brazilian Cerrado soil Actinobacteria ecology. Biomed Res Int 2013:503805

  12. 12.

    Wu N, Zhang Y, Pan H, Zhang J (2010) The role of nonphotosynthetic microbes in the recovery of biological soil crusts in the Gurbantunggut Desert, Northwestern China. Arid Land Res Manag 24:42–56

    Google Scholar 

  13. 13.

    Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol Rev 33:917–941

    CAS  PubMed  Google Scholar 

  14. 14.

    Seviour R, Stasinopoulos S, Auer D, Gibbs P (1992) Production of pullulan and other exopolysaccharides by filamentous fungi. Crc Cr Rev Biotechn 12:279–298

    CAS  Google Scholar 

  15. 15.

    Mahapatra S, Banerjee D (2013) Fungal exopolysaccharide: production, composition and applications. Microbiol Insights 6:1–16

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Suresh Kumar A, Mody K, Jha B (2007) Bacterial exopolysaccharides–a perception. J Basic Microb 47:103–117

    Google Scholar 

  17. 17.

    Zaady E, Kuhn U, Wilske B, Sandoval-Soto L, Kesselmeier J (2000) Patterns of CO2 exchange in biological soil crusts of successional age. Soil Biol Biochem 32:959–966

    CAS  Google Scholar 

  18. 18.

    Fischer T, Gypser S, Subbotina M, Veste M (2014) Synergic hydraulic and nutritional feedback mechanisms control surface patchiness of biological soil crusts on tertiary sands at a post-mining site. J Hydrol Hydromech 62:293–302

    Google Scholar 

  19. 19.

    Fischer T, Veste M (2018) Carbon cycling of biological soil crusts mirrors ecological maturity along a Central European inland dune catena. Catena 160:68–75

    CAS  Google Scholar 

  20. 20.

    West NE (1990) Structure and function of microphytic soil crusts in wildland ecosystems of arid to semi-arid regions. Adv Ecol Res 20:179–223

    Google Scholar 

  21. 21.

    Eldridge D, Greene R (1994) Microbiotic soil crusts-a review of their roles in soil and ecological processes in the rangelands of Australia. Soil Res 32:389–415

    Google Scholar 

  22. 22.

    Kidron G, Barzilay E, Sachs E (2000) Microclimate control upon sand microbiotic crusts, western Negev Desert, Israel. Geomorphology 36:1–18

    Google Scholar 

  23. 23.

    Yair A, Almog R, Veste M (2011) Differential hydrological response of biological topsoil crusts along a rainfall gradient in a sandy arid area: Northern Negev desert, Israel. Catena 87:326–333

    Google Scholar 

  24. 24.

    Kidron GJ, Vonshak A (2012) The use of microbiotic crusts as biomarkers for ponding, subsurface flow and soil moisture content and duration. Geoderma 181:56–64

    Google Scholar 

  25. 25.

    Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178

    CAS  Google Scholar 

  26. 26.

    Schmid J, Sieber V, Rehm B (2015) Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol 6:496

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Pereira SB, Mota R, Santos CL, De Philippis R, Tamagnini P (2013) Assembly and export of extracellular polymeric substances (EPS) in cyanobacteria: a phylogenomic approach. Adv Bot Res 65:235–279

    CAS  Google Scholar 

  28. 28.

    Hunt F (1985) Patterns of LPS synthesis in gram negative bacteria. J Theor Biol 115:213–219

    CAS  PubMed  Google Scholar 

  29. 29.

    Wang X, Quinn PJ (2010) Lipopolysaccharide: biosynthetic pathway and structure modification. Prog Lipid Res 49:97–107

    CAS  PubMed  Google Scholar 

  30. 30.

    Whitfield C, Trent MS (2014) Biosynthesis and export of bacterial lipopolysaccharides. Annu Rev Biochem 83:99–128

    CAS  PubMed  Google Scholar 

  31. 31.

    Costa OY, Raaijmakers JM, Kuramae EE (2018) Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Front Microbiol 9:1–14

    Google Scholar 

  32. 32.

    Mazor G, Kidron GJ, Vonshak A, Abeliovich A (1996) The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiol Ecol 21:121–130

    CAS  Google Scholar 

  33. 33.

    HuiXia P, ZhengMing C, XueMei Z, ShuYong M, XiaoLing Q, Fang W (2007) A study on an oligotrophic bacteria and its ecological characteristics in an arid desert area. Sci China Ser D 50:128–134

    Google Scholar 

  34. 34.

    Colica G, Li H, Rossi F, Li D, Liu Y, De Philippis R (2014) Microbial secreted exopolysaccharides affect the hydrological behavior of induced biological soil crusts in desert sandy soils. Soil Biol Biochem 68:62–70

    CAS  Google Scholar 

  35. 35.

    Kheirfam H, Sadeghi SH, Darki BZ, Homaee M (2017) Controlling rainfall-induced soil loss from small experimental plots through inoculation of bacteria and cyanobacteria. Catena 152:40–46

    CAS  Google Scholar 

  36. 36.

    Mugnai G, Rossi F, Felde VJMNL, Colesie C, Büdel B, Peth S, Kaplan A, De Philippis R (2018) The potential of the cyanobacterium Leptolyngbya ohadii as inoculum for stabilizing bare sandy substrates. Soil Biol Biochem 127:318–328

    CAS  Google Scholar 

  37. 37.

    Cania B, Vestergaard G, Krauss M, Fliessbach A, Schloter M, Schulz S (2019) A long-term field experiment demonstrates the influence of tillage on the bacterial potential to produce soil structure-stabilizing agents such as exopolysaccharides and lipopolysaccharides. Environ Microbiome 1:1–14

    Google Scholar 

  38. 38.

    Gerwin W, Schaaf W, Biemelt D, Fischer A, Winter S, Hüttl RF (2009) The artificial catchment “Chicken Creek”(Lusatia, Germany)—a landscape laboratory for interdisciplinary studies of initial ecosystem development. Ecol Eng 35:1786–1796

    Google Scholar 

  39. 39.

    Russell DJ, Hohberg K, Elmer M (2010) Primary colonisation of newly formed soils by actinedid mites. Soil Org 82:237–251

    Google Scholar 

  40. 40.

    Zaplata MK, Winter S, Fischer A, Kollmann J, Ulrich W (2012) Species-driven phases and increasing structure in early-successional plant communities. Am Nat 181:E17–E27

    PubMed  Google Scholar 

  41. 41.

    Lukešová A (2001) Soil algae in brown coal and lignite post-mining areas in central Europe (Czech Republic and Germany). Restor Ecol 9:341–350

    Google Scholar 

  42. 42.

    Gypser S, Herppich WB, Fischer T, Lange P, Veste M (2016) Photosynthetic characteristics and their spatial variance on biological soil crusts covering initial soils of post-mining sites in Lower Lusatia, NE Germany. Flora 220:103–116

    Google Scholar 

  43. 43.

    Dümig A, Veste M, Hagedorn F, Fischer T, Lange P, Spröte R, Kögel-Knabner I (2014) Organic matter from biological soil crusts induces the initial formation of sandy temperate soils. Catena 122:196–208

    Google Scholar 

  44. 44.

    Fischer T, Veste M, Bens O, Hüttl RF (2012) Dew formation on the surface of biological soil crusts in central European sand ecosystems. Biogeosciences 9:4621–4628

    Google Scholar 

  45. 45.

    Fischer T, Veste M, Eisele A, Bens O, Spyra W, Hüttl RF (2012) Small scale spatial heterogeneity of normalized difference vegetation indices (NDVIs) and hot spots of photosynthesis in biological soil crusts. Flora 207:159–167

    Google Scholar 

  46. 46.

    Döhring T, Koefferlein M, Thiel S, Seidlitz HK (1996) Spectral shaping of artificial UV-B irradiation for vegetation stress research. J Plant Physiol 148:115–119

    Google Scholar 

  47. 47.

    Thiel S, Döhring T, Köfferlein M, Kosak A, Martin P, Seidlitz HK (1996) A phytotron for plant stress research: how far can artificial lighting compare to natural sunlight? J Plant physiol 148:456–463

    CAS  Google Scholar 

  48. 48.

    Brankatschk R, Töwe S, Kleineidam K, Schloter M, Zeyer J (2011) Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield. ISME J 5:1025–1037

    CAS  PubMed  Google Scholar 

  49. 49.

    Fischer T, Veste M, Wiehe W, Lange P (2010) Water repellency and pore clogging at early successional stages of microbiotic crusts on inland dunes, Brandenburg, NE Germany. Catena 80:47–52

    Google Scholar 

  50. 50.

    Hallett P, Young I (1999) Changes to water repellence of soil aggregates caused by substrate-induced microbial activity. Eur J Soil Sci 50:35–40

    Google Scholar 

  51. 51.

    Urbanek E, Hallett P, Feeney D, Horn R (2007) Water repellency and distribution of hydrophilic and hydrophobic compounds in soil aggregates from different tillage systems. Geoderma 140:147–155

    CAS  Google Scholar 

  52. 52.

    Köhne JM, Schlüter S, Vogel H-J (2011) Predicting solute transport in structured soil using pore network models. Vadose Zone J 10:1082–1096

    Google Scholar 

  53. 53.

    Vogel H-J, Weller U, Schlüter S (2010) Quantification of soil structure based on Minkowski functions. Comput Geosci 36:1236–1245

    Google Scholar 

  54. 54.

    Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fert Soils 53:479–484. https://doi.org/10.1007/s00374-017-1191-3

    Article  Google Scholar 

  55. 55.

    Schubert M, Lindgreen S, Orlando L (2016) AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res Notes 9:88

    PubMed  PubMed Central  Google Scholar 

  56. 56.

    Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Schmieder R, Edwards R (2011) Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PloS One 6:e17288

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Rodriguez-R LM, Konstantinidis KT (2014) Estimating coverage in metagenomic data sets and why it matters. ISME J 8:2349–2351

    PubMed  PubMed Central  Google Scholar 

  59. 59.

    Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 7:11257

    CAS  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Kopylova E, Noé L, Touzet H (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28:3211–3217

    CAS  PubMed  Google Scholar 

  61. 61.

    Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M (2015) eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–D293

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Haft DH, Selengut JD, Richter RA, Harkins D, Basu MK, Beck E (2013) TIGRFAMs and genome properties in 2013. Nucleic Acids Res 41:D387–D395

    CAS  PubMed  Google Scholar 

  63. 63.

    Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285

    CAS  PubMed  Google Scholar 

  64. 64.

    Rho M, Tang H, Ye Y (2010) FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res 38:e191–e191

    PubMed  PubMed Central  Google Scholar 

  65. 65.

    Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60

    CAS  PubMed  Google Scholar 

  66. 66.

    R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  67. 67.

    Field A, Miles J, Field Z (2012) Discovering statistics using R. Sage publications, Thousand Oaks

    Google Scholar 

  68. 68.

    Wilcox RR, Schönbrodt FD (2014) The WRS package for robust statistics in R. R package version 0.24. Retrieved from http://r-forge.r-project.org/projects/wrs/

  69. 69.

    Tunks T (1978) The use of omega squared in interpreting statistical significance. B Coun Res Music Ed 57:28–34.

  70. 70.

    Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    CAS  PubMed  Google Scholar 

  71. 71.

    Legendre P, Legendre LF (2012) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  72. 72.

    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) Vegan: community ecology package. R package version 2:5–1

    Google Scholar 

  73. 73.

    Sul WJ, Asuming-Brempong S, Wang Q, Tourlousse DM, Penton CR, Deng Y, Rodrigues JL, Adiku SG, Jones JW, Zhou J (2013) Tropical agricultural land management influences on soil microbial communities through its effect on soil organic carbon. Soil Biol Biochem 65:33–38

    CAS  Google Scholar 

  74. 74.

    Cederlund H, Wessén E, Enwall K, Jones CM, Juhanson J, Pell M, Philippot L, Hallin S (2014) Soil carbon quality and nitrogen fertilization structure bacterial communities with predictable responses of major bacterial phyla. Appl Soil Ecol 84:62–68

    Google Scholar 

  75. 75.

    Coenye T (2014) The family Burkholderiaceae. In: Rosenberg E (ed) The prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Heidelberg, pp 759–776

    Google Scholar 

  76. 76.

    Willems A (2014) The family Comamonadaceae. In: Rosenberg E (ed) The prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Heidelberg, pp 777–851

    Google Scholar 

  77. 77.

    Teixeira LM, Merquior VLC (2014) The family Moraxellaceae. In: Rosenberg E (ed) The prokaryotes: Gammaproteobacteria. Springer, Heidelberg, pp 443–476

    Google Scholar 

  78. 78.

    McBride MJ (2014) The family Flavobacteriaceae. In: Rosenberg E (ed) The prokaryotes: other major lineages of bacteria and the archaea. Springer, Heidelberg, pp 643–676

    Google Scholar 

  79. 79.

    Vogeleer P, Tremblay YD, Mafu AA, Jacques M, Harel J (2014) Life on the outside: role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli. Front Microbiol 5:317

    PubMed  PubMed Central  Google Scholar 

  80. 80.

    Lindhout T, Lau PCY, Brewer D, Lam JS (2009) Truncation in the core oligosaccharide of lipopolysaccharide affects flagella-mediated motility in Pseudomonas aeruginosa PAO1 via modulation of cell surface attachment. Microbiology +155:3449–3460

    PubMed  Google Scholar 

  81. 81.

    Kierek K, Watnick PI (2003) The Vibrio cholerae O139 O-antigen polysaccharide is essential for Ca2+-dependent biofilm development in sea water. Proc Natl Acad Sci U S A 100:14357–14362

    CAS  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Huang Q, Wu H, Cai P, Fein JB, Chen W (2015) Atomic force microscopy measurements of bacterial adhesion and biofilm formation onto clay-sized particles. Sci Rep-UK 5:16857

    CAS  Google Scholar 

  83. 83.

    de Caire GZ, De Cano MS, De Mule MZ, Palma R, Colombo K (1997) Exopolysaccharide of Nostoc muscorum (Cyanobacteria) in the aggregation of soil particles. J Appl Phycol 9:249–253

    Google Scholar 

  84. 84.

    Carrasco L, Caravaca F, Azcón R, Roldán A (2009) Soil acidity determines the effectiveness of an organic amendment and a native bacterium for increasing soil stabilisation in semiarid mine tailings. Chemosphere 74:239–244

    CAS  PubMed  Google Scholar 

  85. 85.

    Rossi F, Li H, Liu Y, De Philippis R (2017) Cyanobacterial inoculation (cyanobacterisation): perspectives for the development of a standardized multifunctional technology for soil fertilization and desertification reversal. Earth-Sci Rev 171:28–43

    Google Scholar 

  86. 86.

    Raanan H, Felde VJ, Peth S, Drahorad S, Ionescu D, Eshkol G, Treves H, Felix-Henningsen P, Berkowicz SM, Keren N (2016) Three-dimensional structure and cyanobacterial activity within a desert biological soil crust. Environ Microbiol 18:372–383

    CAS  PubMed  Google Scholar 

  87. 87.

    Issa OM, Défarge C, Trichet J, Valentin C, Rajot J-L (2009) Microbiotic soil crusts in the Sahel of Western Niger and their influence on soil porosity and water dynamics. Catena 77:48–55

    CAS  Google Scholar 

  88. 88.

    Greene R (1992) Soil physical properties of three geomorphic zones in a semi-arid mulga woodland [Acacia aneura]. Aust J Soil Res 30:55–69

    Google Scholar 

  89. 89.

    Eldridge DJ (2003) Biological soil crusts and water relations in Australian deserts. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 327–337

    Google Scholar 

  90. 90.

    Felde VJMNL, Rossi F, Colesie C, Uteau-Puschmann D, Horne R, Felix-Henningsen P, De Philippis R, Peth S (2016) Pore characteristics in biological soil crusts are independent of extracellular polymeric substances. Soil Biol Biochem 103:294–299

    CAS  Google Scholar 

  91. 91.

    Pluis J (1994) Algal crust formation in the inland dune area, Laarder Wasmeer, the Netherlands. Vegetation 113:41–51

    Google Scholar 

  92. 92.

    Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  93. 93.

    Rossi F, Micheletti E, Bruno L, Adhikary SP, Albertano P, De Philippis R (2012) Characteristics and role of the exocellular polysaccharides produced by five cyanobacteria isolated from phototrophic biofilms growing on stone monuments. Biofouling 28:215–224

    CAS  PubMed  Google Scholar 

  94. 94.

    Colica G, Li H, Rossi F, Philippis RD, Liu Y (2015) Differentiation of the characteristics of excreted extracellular polysaccharides reveals the heterogeneous primary succession of induced biological soil crusts. J Appl Phycol 27:24–32

    Google Scholar 

  95. 95.

    Redmile-Gordon M, Brookes P, Evershed R, Goulding K, Hirsch P (2014) Measuring the soil-microbial interface: extraction of extracellular polymeric substances (EPS) from soil biofilms. Soil Biol Biochem 72:163–171

    CAS  Google Scholar 

  96. 96.

    Lagier J-C, Million M, Hugon P, Armougom F, Raoult D (2012) Human gut microbiota: repertoire and variations. Front Cell Infect Mi 2:136

    Google Scholar 

  97. 97.

    Antunes LCS, Poppleton D, Klingl A, Criscuolo A, Dupuy B, Brochier-Armanet C, Beloin C, Gribaldo S (2016) Phylogenomic analysis supports the ancestral presence of LPS-outer membranes in the Firmicutes. Elife 5:e14589

    PubMed  PubMed Central  Google Scholar 

  98. 98.

    Poppleton DI, Duchateau M, Hourdel V, Matondo M, Flechsler J, Klingl A, Beloin C, Gribaldo S (2017) Outer membrane proteome of Veillonella parvula: a diderm Firmicute of the human microbiome. Front Microbiol 8:1215

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Whitfield C, Larue K (2008) Stop and go: regulation of chain length in the biosynthesis of bacterial polysaccharides. Nat Struct Mol Biol 15:121–123

    CAS  PubMed  Google Scholar 

  100. 100.

    Whitfield C (2010) Polymerases: glycan chain-length control. Nat Chem Biol 6:403–404

    CAS  PubMed  Google Scholar 

  101. 101.

    Rosenow C, Esumeh F, Roberts IS, Jann K (1995) Characterization and localization of the KpsE protein of Escherichia coli K5, which is involved in polysaccharide export. J Bacteriol 177:1137–1143

    CAS  PubMed  PubMed Central  Google Scholar 

  102. 102.

    Bachtiar BM, Coloe PJ, Fry BN (2007) Knockout mutagenesis of the kpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium–host interactions. FEMS Immunol Med Mic 49:149–154

    CAS  Google Scholar 

  103. 103.

    Muhammadi AN (2007) Genetics of bacterial alginate: alginate genes distribution, organization and biosynthesis in bacteria. Curr Genomics 8:191–202

    CAS  PubMed  PubMed Central  Google Scholar 

  104. 104.

    Rendueles O, Garcia-Garcerà M, Néron B, Touchon M, Rocha EP (2017) Abundance and co-occurrence of extracellular capsules increase environmental breadth: implications for the emergence of pathogens. PLoS Pathog 13:e1006525

    PubMed  PubMed Central  Google Scholar 

  105. 105.

    Putker F, Bos MP, Tommassen J (2015) Transport of lipopolysaccharide to the Gram-negative bacterial cell surface. FEMS Microbiol Rev 39:985–1002

    CAS  PubMed  Google Scholar 

  106. 106.

    Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ (2008) Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A 105:5537–5542

    CAS  PubMed  PubMed Central  Google Scholar 

  107. 107.

    Benedet M, Falchi FA, Puccio S, Di Benedetto C, Peano C, Polissi A, Dehò G (2016) The lack of the essential LptC protein in the trans-envelope lipopolysaccharide transport machine is circumvented by suppressor mutations in LptF, an inner membrane component of the Escherichia coli transporter. PloS One 11:e0161354

    PubMed  PubMed Central  Google Scholar 

  108. 108.

    Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519

    CAS  PubMed  PubMed Central  Google Scholar 

  109. 109.

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    CAS  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Wilhelm RC, Niederberger TD, Greer C, Whyte LG (2011) Microbial diversity of active layer and permafrost in an acidic wetland from the Canadian High Arctic. Can J Microbiol 57:303–315

    CAS  PubMed  Google Scholar 

  112. 112.

    Santofimia E, González-Toril E, López-Pamo E, Gomariz M, Amils R, Aguilera Á (2013) Microbial diversity and its relationship to physicochemical characteristics of the water in two extreme acidic pit lakes from the Iberian Pyrite Belt (SW Spain). PLoS One 8:e66746

    CAS  PubMed  PubMed Central  Google Scholar 

  113. 113.

    Jones DS, Lapakko KA, Wenz ZJ, Olson MC, Roepke EW, Sadowsky MJ, Novak PJ, Bailey JV (2017) Novel microbial assemblages dominate weathered sulfide-bearing rock from copper-nickel deposits in the Duluth complex, Minnesota, USA. Appl Environ Microbiol 83:e00909–e00917

    CAS  PubMed  PubMed Central  Google Scholar 

  114. 114.

    Kielak AM, Castellane TC, Campanharo JC, Colnago LA, Costa OY, Da Silva MLC, Van Veen JA, Lemos EG, Kuramae EE (2017) Characterization of novel Acidobacteria exopolysaccharides with potential industrial and ecological applications. Sci Rep-UK 7:41193

    CAS  Google Scholar 

  115. 115.

    Rampadarath S, Bandhoa K, Puchooa D, Jeewon R, Bal S (2017) Early bacterial biofilm colonizers in the coastal waters of Mauritius. Electron J Biotechn 29:13–21

    CAS  Google Scholar 

  116. 116.

    Prieto-Barajas CM, Valencia-Cantero E, Santoyo G (2017) Microbial mat ecosystems: structure types, functional diversity, and biotechnological application. Electron J Biotechn 31:48–56

    Google Scholar 

  117. 117.

    Mogul R, Vaishampayan P, Bashir M, McKay CP, Schubert K, Bornaccorsi R, Gomez E, Tharayil S, Payton G, Capra J (2017) Microbial community and biochemical dynamics of biological soil crusts across a gradient of surface coverage in the central Mojave desert. Front Microbiol 8:1974

    PubMed  PubMed Central  Google Scholar 

  118. 118.

    De Vries M, Schöler A, Ertl J, Xu Z, Schloter M (2015) Metagenomic analyses reveal no differences in genes involved in cellulose degradation under different tillage treatments. FEMS Microbiol Ecol 91:fiv069

    PubMed  Google Scholar 

  119. 119.

    Wooley JC, Godzik A, Friedberg I (2010) A primer on metagenomics. PLoS Comput Biol 6:1–13

    Google Scholar 

  120. 120.

    Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590

    CAS  PubMed  Google Scholar 

  121. 121.

    Lammel DR, Barth G, Ovaskainen O, Cruz LM, Zanatta JA, Ryo M, de Souza EM, Pedrosa FO (2018) Direct and indirect effects of a pH gradient bring insights into the mechanisms driving prokaryotic community structures. Microbiome 6:106

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Gudrun Hufnagel for measuring the biochemical parameters, Christoph Schmidt and Abilash Chakravarthy Durai Raj for bioinformatical advice, and Viviane Radl and Antonios Michas for constructive feedback on the previous version of the manuscript. This study was performed as part of the Transregional Collaborative Research Centre 38 (SFB/TRR 38), which is financially supported by the Deutsche Forschungsgemeinschaft (DFG, Bonn) and the Brandenburg Ministry of Science, Research and Culture (MWFK, Potsdam), and the project “The influence of agricultural management practices on microbial functions and networks in biological soil crusts” funded by the DFG in frame of the DFG-Nachwuchsakademie “Agrarökosystemforschung: Bodenressourcen und Pflanzenproduktion.” The authors also gratefully acknowledge the funding provided by the German Federal Office for Agriculture and Food (BLE).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Stefanie Schulz.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic Supplementary Material

ESM 1

Supplementary figures S1-8 (PDF 1664 kb)

ESM 2

Supplementary tables S1-5 (PDF 347 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cania, B., Vestergaard, G., Kublik, S. et al. Biological Soil Crusts from Different Soil Substrates Harbor Distinct Bacterial Groups with the Potential to Produce Exopolysaccharides and Lipopolysaccharides. Microb Ecol 79, 326–341 (2020). https://doi.org/10.1007/s00248-019-01415-6

Download citation

Keywords

  • Biological soil crusts
  • Exopolysaccharides
  • Lipopolysaccharides
  • Microbiome
  • Metagenomics