Abstract
Biological soil crusts (biocrusts) are distributed in arid and semiarid regions across the globe. Microorganisms are an essential component in biocrusts. They add and accelerate critical biochemical processes. However, little is known about the functional genes and metabolic processes of microbiomes in lichen and moss biocrust. This study used shotgun metagenomic sequencing to compare the microbiomes of lichen-dominated and moss-dominated biocrust and reveal the microbial genes and metabolic pathways involved in carbon and nitrogen cycling. The results showed that Actinobacteria, Bacteroidetes, and Acidobacteria were more abundant in moss biocrust than lichen biocrust, while Proteobacteria and Cyanobacteria were more abundant in lichen biocrust than moss biocrust. The relative abundance of carbohydrate-active enzymes and enzymes associated with carbon and nitrogen metabolism differed significantly between microbiomes of the two biocrust types. However, in the microbial communities of both biocrust types, respiration pathways dominated over carbon fixation pathways. The genes encoding carbon monoxide dehydrogenase were more abundant than those encoding ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCo) involved in carbon fixation. Similarly, metabolic N-pathway diversity was dominated by nitrogen reduction, followed by denitrification, with nitrogen fixation the lowest proportion. Gene diversity involved in N cycling differed between the microbiomes of the two biocrust types. Assimilatory nitrate reduction genes had higher relative abundance in lichen biocrust, whereas dissimilatory nitrate reduction genes had higher relative abundance in moss biocrust. As dissolved organic carbon and soil organic carbon are considered the main drivers of the community structure in the microbiome of biocrust, these results indicate that biocrust type has a pivotal role in microbial diversity and related biogeochemical cycling.
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Data Availability
All data is publicly available on the SRA database under BioProject PRJNA793166.
References
Millennium Ecosystem Assessment Board (2005) Ecosystems and human well-being: synthesis. Island Press, Washington, DC
Belnap J, Lange OL (2003) Biological soil crusts: structure, function, and management. Springer-Verlag, Berlin
Eldridge D (2000) Ecology and management of biological soil crusts: recent developments and future challenges. Bryologist 103:742–747. https://doi.org/10.1639/0007-2745(2000)103[0742:Eamobs]2.0.Co;2
Lan S, Wu L, Zhang D, Hu C (2012) Successional stages of biological soil crusts and their microstructure variability in Shapotou region (China). Environ Earth Sci 65:77–88. https://doi.org/10.1007/s12665-011-1066-0
Lan S, Wu L, Zhang D, Hu C (2013) Assessing level of development and successional stages in biological soil crusts with biological indicators. Microb Ecol 66:394–403. https://doi.org/10.1007/s00248-013-0191-6
Maestre FT, Salguero-Gomez R, Quero JL (2012) It is getting hotter in here: determining and projecting the impacts of global environmental change on drylands introduction. Philos T R Soc B 367:3062–3075. https://doi.org/10.1098/rstb.2011.0323
Weber B, Wu D, Tamm A, Ruckteschler N, Rodriguez-Caballero E, Steinkamp J, Meusel H, Elbert W, Behrendt T, Soergel M, Cheng Y, Crutzen PJ, Su H, Poeschi U (2015) Biological soil crusts accelerate the nitrogen cycle through large NO and HONO emissions in drylands. P Natl Acad Sci USA 112:15384–15389. https://doi.org/10.1073/pnas.1515818112
Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. P Natl Acad Sci USA 109:21390–21395. https://doi.org/10.1073/pnas.1215210110
Comeau AM, Douglas GM, Langille MGI (2017) Microbiome helper: a custom and streamlined workflow for microbiome research. Msystems 2:e00127-00116. https://doi.org/10.1128/mSystems.00127-16
Elbert W, Weber B, Burrows S, Steinkamp J, Buedel B, Andreae MO, Poeschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462. https://doi.org/10.1038/ngeo1486
Zhao M, Heinsch FA, Nemani RR, Running SW (2005) Improvements of the MODIS terrestrial gross and net primary production global data set. Remote Sens Environ 95:164–176. https://doi.org/10.1016/j.rse.2004.12.011
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth’s nitrogen cycle. Science 330:192–196. https://doi.org/10.1126/science.1186120
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vorosmarty CJ (2004) Nitrogen cycles: past, present and future. Biogeochemistry 70:153–226. https://doi.org/10.1007/s10533-004-0370-0
Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, Garcia-Palacios P (2011) Biological soil crust microsites are the main contributor to soil respiration in a semiarid ecosystem. Ecosystems 14:835–847. https://doi.org/10.1007/s10021-011-9449-3
Darby BJ, Neher DA, Belnap J (2010) Impact of biological soil crusts and desert plants on soil microfaunal community composition. Plant Soil 328:421–431. https://doi.org/10.1007/s11104-009-0122-y
Kuske CR, Yeager CM, Johnson S, Ticknor LO, Belnap J (2012) Response and resilience of soil biocrust bacterial communities to chronic physical disturbance in arid shrublands. Isme J 6:886–897. https://doi.org/10.1038/ismej.2011.153
Housman DC, Powers HH, Collins AD, Belnap J (2006) Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert. J Arid Environ 66:620–634. https://doi.org/10.1016/j.jaridenv.2005.11.014
Li XR, Zhang P, Su YG, Jia RL (2012) Carbon fixation by biological soil crusts following revegetation of sand dunes in arid desert regions of China: a four-year field study. CATENA 97:119–126. https://doi.org/10.1016/j.catena.2012.05.009
Su YG, Zhao X, Li AX, Li XR, Huang G (2011) Nitrogen fixation in biological soil crusts from the Tengger desert, northern China. Eur J Soil Biol 47:182–187. https://doi.org/10.1016/j.ejsobi.2011.04.001
Wang IG, Zhao YG, Xu MX, Yang LN, Ming J (2013) Effects of biological soil crust at different succession stages in hilly region of Loess Plateau on soil CO2 flux. Chinese J Appl Eco 24:659–666. https://doi.org/10.13287/j.1001-9332.2013.0208
Liu LC, Liu YB, Zhang P, Song G, Hui R, Wang ZR, Wang J (2017) Development of bacterial communities in biological soil crusts along a revegetation chronosequence in the Tengger Desert, northwest China. Biogeosciences 14:3801–3814. https://doi.org/10.5194/bg-14-3801-2017
Abed RMM, Lam P, de Beer D, Stief P (2013) High rates of denitrification and nitrous oxide emission in arid biological soil crusts from the Sultanate of Oman. Isme J 7:1862–1875. https://doi.org/10.1038/ismej.2013.55
Delgado-Baquerizo M, Maestre FT, Gallardo A (2013) Biological soil crusts increase the resistance of soil nitrogen dynamics to changes in temperatures in a semi-arid ecosystem. Plant Soil 366:35–47. https://doi.org/10.1007/s11104-012-1404-3
Zhou H, Gao Y, Jia XH, Wang MM, Ding JJ, Chen L, Bao F, Wu B (2020) Network analysis reveals the strengthening of microbial interaction in biological soil crust development in the Mu Us Sandy Land, northwestern China. Soil Biol Biochem 144:107782. https://doi.org/10.1016/j.soilbio.2020.107782
Li JY, Jin XY, Zhang XC, Chen L, Liu JL, Zhang HM, Zhang X, Zhang YF, Zhao JH, Ma ZS, Jin D (2020) Comparative metagenomics of two distinct biological soil crusts in the Tengger Desert. China Soil Biol Biochem 140:107637. https://doi.org/10.1016/j.soilbio.2019.107637
Miralles I, Ortega R, Montero-Calasanz MC (2021) Studying the microbiome of cyanobacterial biocrusts from drylands and its functional influence on biogeochemical cycles. Res Square Prepr. https://doi.org/10.21203/rs.3.rs-252045/v1
Hu R, Wang XP, Pan YX, Zhang YF, Zhang H, Chen N (2015) Seasonal variation of net N mineralization under different biological soil crusts in Tengger Desert, North China. CATENA 127:9–16. https://doi.org/10.1016/j.catena.2014.12.012
Jia X, Zha TS, Wu B, Zhang YQ, Gong JN, Qin SG, Chen GP, Qian D, Kellomaki S, Peltola H (2014) Biophysical controls on net ecosystem CO2 exchange over a semiarid shrubland in northwest China. Biogeosciences 11:4679–4693. https://doi.org/10.5194/bg-11-4679-2014
Lai ZR, Zhang YQ, Liu JB, Wu B, Qin SG, Fa KY (2016) Fine-root distribution, production, decomposition, and effect on soil organic carbon of three revegetation shrub species in northwest China. Forest Ecol Manag 359:381–388. https://doi.org/10.1016/j.foreco.2015.04.025
Walkley AJ, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38. https://doi.org/10.1097/00010694-193401000-00003
Gregorich EG, Wen G, Voroney RP, Kachanoski RG (1990) Calibration of a rapid direct chloroform extraction method for measuring soil microbial biomass C. Soil Biol Biochem 22:1009–1011. https://doi.org/10.1016/0038-0717(90)90148-S
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. https://doi.org/10.1016/0038-0717(85)90144-0
Wang HL, Sun L (2018) Comparative metagenomic analysis of the microbial communities in the surroundings of Iheya north and Iheya ridge hydrothermal fields reveals insights into the survival strategy of microorganisms in deep-sea environments. J Mar Syst 180:102–111. https://doi.org/10.1016/j.jmarsys.2016.10.006
Luo RB, Liu BH, Xie YL, Li ZY, Huang WH, Yuan JY, He GZ, Chen YX, Pan Q, Liu YJ, Tang JB, Wu GX, Zhang H, Shi YJ, Liu Y, Yu C, Wang B, Lu Y, Han CL, Cheung DW, Yiu SM, Peng SL, Zhu XQ, Liu GM, Liao XK, Li YR, Yang HM, Wang J, Lam T-W, Wang J (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18. https://doi.org/10.1186/2047-217x-1-18
Li JH, Jia HJ, Cai XH, Zhong HZ, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, Juncker AS, Manichanh C, Chen B, Zhang WW, Levenez F, Wang J, Xu X, Xiao L, Liang SS, Zhang DY, Zhang ZX, Chen WN, Zhao HL, Al-Aama JY, Edris S, Yang HM, Wang J, Hansen T, Nielsen HB, Brunak S, Kristiansen K, Guarner F, Pedersen O, Dore J, Ehrlich SD, Bork P, Wang J, Meta HITC (2014) An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 32:834–841. https://doi.org/10.1038/nbt.2942
Huson DH, Mitra S, Ruscheweyh H-J, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21:1552–1560. https://doi.org/10.1101/gr.120618.111
Karlsson FH, Tremaroli V, Nookaew I, Bergstrom G, Behre CJ, Fagerberg B, Nielsen J, Backhed F (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498:99–103. https://doi.org/10.1038/nature12198
Altschul S, Madden T, Schaffer A, Zhang JH, Zhang Z, Miller W, Lipman D (1998) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Faseb J 12:A1326–A1326. https://doi.org/10.1093/nar/25.17.3389
Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J (2017) Microbiome analyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188. https://doi.org/10.1093/nar/gkx295
Chong J, Liu P, Zhou G, Xia J (2020) Using microbiome analyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat Protoc 15:799–821. https://doi.org/10.1038/s41596-019-0264-1
Chen C, Chen H, Zhang Y, Thomas HR, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Miralles I, Trasar-Cepeda C, Leirós M, Gil-Sotres F (2013) Labile carbon in biological soil crusts in the Tabernas desert, SE Spain. Soil Biol Biochem 58:1–8. https://doi.org/10.1016/j.soilbio.2012.11.010
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. https://doi.org/10.1128/aem.00335-09
Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2:94. https://doi.org/10.3389/fmicb.2011.00094
Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129. https://doi.org/10.1111/j.1574-6976.2012.00343.x
Kuramae EE, Etienne Y, Wong LC, Pijl AS, Van VJA, Kowalchuk GA (2015) Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol 79:12–24. https://doi.org/10.1111/j.1574-6941.2011.01192.x
Canfora L, Bacci G, Pinzari F, Lo Papa G, Dazzi C, Benedetti A (2014) Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a saline soil? PLoS ONE 9:e106662. https://doi.org/10.1371/journal.pone.0106662
Tian C, Xi J, Ju MC, Li YH, Guo Q, Yao L, Wang C, Lin YB, Li Q, Williams WJ, Bu CF (2021) Biocrust microbiomes influence ecosystem structure and function in the Mu Us Sandland, northwest China. Ecol Inform 66:101441. https://doi.org/10.1016/j.ecoinf.2021.101441
Yu TT, Li M, Niu MY, Fan XB, Liang WY, Wang FP (2018) Difference of nitrogen-cycling microbes between shallow bay and deep-sea sediments in the South China Sea. Appl Microbiol Biotechnol 102:447–459. https://doi.org/10.1007/s00253-017-8594-9
Vetrovsky T, Steffen KT, Baldrian P (2014) Potential of cometabolic transformation of polysaccharides and lignin in lignocellulose by soil Actinobacteria. PLoS ONE 9:e89108. https://doi.org/10.1371/journal.pone.0089108
Qiao S, Bao L, Wang K, Sun S, Liu H (2020) Activation of a specific gut Bacteroides-folate-liver axis benefits for the alleviation of nonalcoholic hepatic steatosis. Cell Rep 32:108005. https://doi.org/10.1016/j.celrep.2020.108005
Pankratov TA, Ivanova AO, Dedysh SN, Liesack W (2011) Bacterial populations and environmental factors controlling cellulose degradation in an acidic Sphagnum peat. Environ Microbiol 13:1800–1814. https://doi.org/10.1111/j.1462-2920.2011.02491.x
Gundlapally SR, Garcia-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol 52:345–357. https://doi.org/10.1007/s00248-006-9011-6
Pepe-Ranney C, Koechli C, Potrafka R, Andam C, Eggleston E, Garcia-Pichel F, Buckley DH (2016) Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation. Isme J 10:287–298. https://doi.org/10.1038/ismej.2015.106
Kidron GJ, Vonshak A, Abeliovich A (2008) Recovery rates of microbiotic crusts within a dune ecosystem in the Negev Desert. Geomorphology 100:444–452. https://doi.org/10.1016/j.geomorph.2008.01.012
Abed RMM, Al Kharusi S, Schramm A, Robinson MD (2010) Bacterial diversity, pigments and nitrogen fixation of biological desert crusts from the Sultanate of Oman. FEMS Microbiol Ecol 72:418–428. https://doi.org/10.1111/j.1574-6941.2010.00854.x
Phuong Thi L, Makhalanyane TP, Guerrero LD, Vikram S, Van de Peer Y, Cowan DA (2016) Comparative metagenomic analysis reveals mechanisms for stress response in hypoliths from extreme hyperarid deserts. Genome Biol Evol 8:2737–2747. https://doi.org/10.1093/gbe/evw189
Chilton AM, Neilan BA, Eldridge DJ (2018) Biocrust morphology is linked to marked differences in microbial community composition. Plant Soil 429:65–75. https://doi.org/10.1007/s11104-017-3442-3
Liu Y, Zhao L, Wang Z, Liu L, Zhang P, Sun J, Wang B, Song G, Li X (2018) Changes in functional gene structure and metabolic potential of the microbial community in biological soil crusts along a revegetation chronosequence in the Tengger Desert. Soil Biol Biochem 126:40–48. https://doi.org/10.1016/j.soilbio.2018.08.012
Zhao LN, Liu YB, Wang ZR, Yuan SW, Qi JH, Zhang WL, Wang YS, Li XR (2020) Bacteria and fungi differentially contribute to carbon and nitrogen cycles during biological soil crust succession in arid ecosystems. Plant Soil 447:379–392. https://doi.org/10.1007/s11104-019-04391-5
Suchao MA, Yilang W, Hongyi AO, Gongliang YU, Renhui LI (2019) A newly recorded cyanobacterial genus Geminocystis in China and its taxonomic and ecological notes. J Lake Sci 31:236–242. https://doi.org/10.18307/2019.0122
Duan QQ, Yang XH, Huang XZ (2017) The diversity of microbial resources in ecological mulberry rhizosphere soil in a rocky desertification area. J Southwest Univ (Nat Sci Ed) 39:25–29. https://doi.org/10.13718/j.cnki.xdzk.2017.07.004
Saul DJ, Aislabie JM, Brown CE, Harris L, Foght JM (2005) Hydrocarbon contamination changes the bacterial diversity of soil from around Scott Base, Antarctica. FEMS Microbiol Ecol 53:141–155. https://doi.org/10.1016/j.femsec.2004.11.007
Mager DM, Thomas AD (2011) Extracellular polysaccharides from cyanobacterial soil crusts: a review of their role in dryland soil processes. J Arid Environ 75:91–97. https://doi.org/10.1016/j.jaridenv.2010.10.001
Mager DM (2010) Carbohydrates in cyanobacterial soil crusts as a source of carbon in the southwest Kalahari, Botswana. Soil Biol Biochem 42:313–318. https://doi.org/10.1016/j.soilbio.2009.11.009
Corfield AP, Berry M (2015) Glycan variation and evolution in the eukaryotes. Trends Biochem Sci 40:351–359. https://doi.org/10.1016/j.tibs.2015.04.004
Adam PS, Borrel G, Gribaldo S (2018) Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes. P Natl Acad Sci USA 115:E1166–E1173. https://doi.org/10.1073/pnas.1716667115
Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, Montgomery K, Lines T, Beardall J, van Dorst J, Snape I, Stott MB, Hugenholtz P, Ferrari BC (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 552:400–403. https://doi.org/10.1038/nature25014
King GM, Weber CF (2007) Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 5:107–118. https://doi.org/10.1038/nrmicro1595
Wang C, Wang XB, Liu DW, Wu HH, Lu XT, Fang YT, Cheng WX, Luo WT, Jiang P, Shi J, Yin HQ, Zhou JZ, Han XG, Bai E (2014) Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat Commun 5:4799. https://doi.org/10.1038/ncomms5799
Kidron GJ, Posmanik R, Brunner T, Nejidat A (2015) Spatial abundance of microbial nitrogen-transforming genes and inorganic nitrogen in biocrusts along a transect of an arid sand dune in the Negev Desert. Soil Biol Biochem 83:150–159. https://doi.org/10.1016/j.soilbio.2015.01.024
Ghaly AE, Ramakrishnan VV (2015) Nitrogen sources and cycling in the ecosystem and its role in air, water and soil pollution: a critical review. J Poullut Eff Control 3:136. https://doi.org/10.4172/2375-4397.1000136
Strauss SL, Day TA, Garcia-Pichel F (2012) Nitrogen cycling in desert biological soil crusts across biogeographic regions in the southwestern United States. Biogeochemistry 108:171–182. https://doi.org/10.1007/s10533-011-9587-x
Yang YF, Gao Y, Wang SP, Xu DP, Yu H, Wu LW, Lin QY, Hu YG, Li XZ, He ZL, Deng Y, Zhou JZ (2014) The microbial gene diversity along an elevation gradient of the Tibetan grassland. Isme J 8:430–440. https://doi.org/10.1038/ismej.2013.146
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We thank all people involved in the maintenance of the experiment. This research was funded by the National Natural Scientific Foundation of China (41971131) and the National Key Research and Development Program of China (2016YFE0203400, 2017YFC0504703).
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Chongfeng Bu conceived the ideas and designed the methodology; Chang Tian, Jingwen Pang, Yahong Li, and Qi Guo collected the data; Chang Tian and Jingwen Pang analyzed the data and wrote the manuscript; Shufang Wu, Hao Bai, and Kadambot H.M. Siddique contributed critically to the manuscript. All authors gave final approval for publication.
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Tian, C., Pang, J., Bu, C. et al. The Microbiomes in Lichen and Moss Biocrust Contribute Differently to Carbon and Nitrogen Cycles in Arid Ecosystems. Microb Ecol 86, 497–508 (2023). https://doi.org/10.1007/s00248-022-02077-7
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DOI: https://doi.org/10.1007/s00248-022-02077-7