Divergent microbial communities in groundwater and overlying soils exhibit functional redundancy for plant-polysaccharide degradation

被引:27
作者
Taubert, Martin [1 ]
Staehly, Jan [1 ]
Kolb, Steffen [1 ,2 ]
Kuesel, Kirsten [1 ,3 ]
机构
[1] Friedrich Schiller Univ Jena, Inst Biodivers, Aquat Geomicrobiol, Jena, Germany
[2] Leibniz Ctr Agr Landscape Res ZALF, Microbial Biogeochem, RA Landscape Proc, Muncheberg, Germany
[3] German Ctr Integrat Biodivers Res iDiv, Leipzig, Germany
来源
PLOS ONE | 2019年 / 14卷 / 03期
关键词
PRISTINE LIMESTONE AQUIFERS; ENZYME-ACTIVITIES; METABOLIC-RESPONSES; ORGANIC-MATTER; BACTERIA; TRANSPORT; ABUNDANCE; DIVERSITY; KINETICS; ECOLOGY;
D O I
10.1371/journal.pone.0212937
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Light driven primary production by plants is the main source of biomass in terrestrial ecosystems. But also in subsurface habitats like aquifers, life is fueled largely by this plant-derived biomass. Here, we investigate the degradation of plant-derived polysaccharides in a groundwater microbiome to identify the microbial key players involved, and compare them to those from soil of the groundwater recharge area. We quantified the activities of enzymes degrading the abundant plant polymers starch, cellulose and hemicellulose in oligotrophic groundwater samples, despite the low cell numbers present. Normalized to 16S rRNA gene copy numbers, these activities were only one order of magnitude lower than in soil. Stimulation of the groundwater microbiome with either starch or cellulose and hemicellulose led to changes of the enzymatic activity ratios, indicating autochthonous production of enzymes in response to the plant polymers. Furthermore, DNA stable isotope probing with C-13 labelled plant polymers allowed us to identify microbes involved in the degradation of these compounds. In (hemi)cellulose microcosms, Bacteroidia and Candidatus Parcubacteria were active, while the active community in starch microcosms mostly comprised Candidatus Saccharibacteria, Cytophagia, and Actinobacteria. Not a single one of the active OTUs was also found to be labelled in soil microcosms. This indicates that the degradation of plant-derived polysaccharides in groundwater is driven by organisms completely distinct from those active in soil. The involvement of members of the candidate phyla Cand. Parcubacteria and Cand. Saccharibacteria, organisms known to be abundant in groundwater, in plant-derived organic matter degradation might strongly impact subsurface carbon cycling.
引用
收藏
页数:19
相关论文
共 71 条
  • [61] Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen
    Schellenberger, Stefanie
    Kolb, Steffen
    Drake, Harold L.
    [J]. ENVIRONMENTAL MICROBIOLOGY, 2010, 12 (04) : 845 - 861
  • [62] Functional microbial community response to nutrient pulses by artificial groundwater recharge practice in surface soils and subsoils
    Schuetz, Kirsten
    Kandeler, Ellen
    Nagel, Peter
    Scheu, Stefan
    Ruess, Liliane
    [J]. FEMS MICROBIOLOGY ECOLOGY, 2010, 72 (03) : 445 - 455
  • [63] Schwab VF, 2016, BIOGEOSCIENCES DISCU, DOI DOI 10.5194/BG-2016-442
  • [64] Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea
    Sowell, Sarah M.
    Wilhelm, Larry J.
    Norbeck, Angela D.
    Lipton, Mary S.
    Nicora, Carrie D.
    Barofsky, Douglas F.
    Carlson, Craig A.
    Smith, Richard D.
    Giovanonni, Stephen J.
    [J]. ISME JOURNAL, 2009, 3 (01) : 93 - 105
  • [65] rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development
    Stoddard, Steven F.
    Smith, Byron J.
    Hein, Robert
    Roller, Benjamin R. K.
    Schmidt, Thomas M.
    [J]. NUCLEIC ACIDS RESEARCH, 2015, 43 (D1) : D593 - D598
  • [66] Taubert M, 2017, ENVIRON MICROBIOL
  • [67] Microbial hydrolysis of polysaccharides
    Warren, RAJ
    [J]. ANNUAL REVIEW OF MICROBIOLOGY, 1996, 50 : 183 - 212
  • [68] Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer
    Wrighton, Kelly C.
    Castelle, Cindy J.
    Wilkins, Michael J.
    Hug, Laura A.
    Sharon, Itai
    Thomas, Brian C.
    Handley, Kim M.
    Mullin, Sean W.
    Nicora, Carrie D.
    Singh, Andrea
    Lipton, Mary S.
    Long, Philip E.
    Williams, Kenneth H.
    Banfield, Jillian F.
    [J]. ISME JOURNAL, 2014, 8 (07) : 1452 - 1463
  • [69] Soil Microbe Active Community Composition and Capability of Responding to Litter Addition after 12 Years of No Inputs
    Yarwood, Stephanie
    Brewer, Elizabeth
    Yarwood, Rockie
    Lajtha, Kate
    Myrold, David
    [J]. APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2013, 79 (04) : 1385 - 1392
  • [70] SIPSim: A Modeling Toolkit to Predict Accuracy and Aid Design of DNA-SIP Experiments
    Youngblut, Nicholas D.
    Barnett, Samuel E.
    Buckley, Daniel H.
    [J]. FRONTIERS IN MICROBIOLOGY, 2018, 9