SpringerLink
Log in

Soil Chemistry and Nutrients Influence the Distribution of Aerobic Anoxygenic Phototrophic Bacteria and Eukaryotic Phototrophic Microorganisms of Physical Soil Crusts at Different Elevations on the Tibetan Plateau

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Photosynthetic microorganisms are widely distributed in the soil and play an important role in plant-free soil crusts. However, the distribution and environmental drivers of phototrophic microbial communities in physical soil crusts, where the abundance of cyanobacteria is low, are scarcely understood. Here, we performed high-throughput sequencing of pufM and 18S rRNA genes in soil crusts at different elevations on the Tibetan Plateau and used the data combined with environmental variables to analyze the diversity and structure of phototrophic microbial communities. We found that the dominant taxa of aerobic anoxygenic phototrophic bacteria (AAPB) and eukaryotic phototrophic microorganisms (EPM) were shown to shift with elevation. The phototrophic microbial diversity showed a single-peak pattern, with the lowest diversity of AAPB and highest diversity of EPM at middle elevations. Moreover, the elevation and soil property determined the phototrophic microbial community. Soil salts, especially Cl−, were the most important for AAPB. Likewise, soil nutrients, especially carbon, were the most important for EPM. The relationship between high-abundance taxa and environmental variables showed that Rhizobiales was significantly negatively correlated with salt ions and positively correlated with chlorophyll. Rhodobacterales showed the strongest and significant positive associations with Cl−. Chlorophyceae and Bacillariophyceae were positively correlated with CO32−. These results indicated that salinity and soil nutrients affected the diversity and structure of microbial communities. This study contributes to our understanding of the diversity, composition, and structure of photosynthetic microorganisms in physical soil crusts and helps in develo** new approaches for controlling desertification and salinization and improving the desert ecological environment.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The data that support the findings of this study are available from the corresponding author upon request. All sequence data generated by this study have been submitted to the NCBI Short Read Archive under BioProject PRJNA669450 with accession number SUB8323950.

References

  1. 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. https://doi.org/10.1016/S0065-2504(08)60055-0

    Article  Google Scholar 

  2. Belnap J, Weber B, Büdel B (2016) In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer, Cham, pp 3–13. https://doi.org/10.1007/978-3-319-30214-0_1

    Chapter  Google Scholar 

  3. Ferrenberg S, Reed SC, Belnap J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. Proc Natl Acad Sci U S A 112(39):12116–12121. https://doi.org/10.1073/pnas.1509150112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Leung PM, Bay SK, Meier DV, Chiri E, Cowan DA, Gillor O, Woebken D, Greening C (2020). mSystems 5(2):e00495–e00419. https://doi.org/10.1128/mSystems.00495-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Li H, Huo D, Wang W, Chen Y, Cheng X, Yu G, Li R (2020) Multifunctionality of biocrusts is positively predicted by network topologies consistent with interspecies facilitation. Mol Ecol 29(8):1560–1573. https://doi.org/10.1111/mec.15424

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14(11):488–496. https://doi.org/10.1016/j.tim.2006.09.001

    Article  CAS  PubMed  Google Scholar 

  7. Csotonyi JT, Swiderski J, Stackebrandt E, Yurkov VV (2008) Novel halophilic aerobic anoxygenic phototrophs from a Canadian hypersaline spring system. Extremophiles 12(4):529–539. https://doi.org/10.1007/s00792-008-0156-8

    Article  CAS  PubMed  Google Scholar 

  8. Ooms MD, Dinh CT, Sargent EH, Sinton D (2016) Photon management for augmented photosynthesis. Nat Commun 7:12699. https://doi.org/10.1038/ncomms12699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. VanInsberghe D, Maas KR, Cardenas E, Strachan CR, Hallam SJ, Mohn WW (2015) Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils. ISME J 9(11):2435–2441. https://doi.org/10.1038/ismej.2015.54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Tahon G, Tytgat B, Stragier P, Willems A (2016) Analysis of cbbL, nifH, and pufLM in Soils from the Sør Rondane Mountains, Antarctica, Reveals a Large Diversity of Autotrophic and Phototrophic Bacteria. Microb Ecol 71(1):131–149. https://doi.org/10.1007/s00248-015-0704-6

    Article  PubMed  Google Scholar 

  11. Yurkov V, Csotonyi J (2009) In: The purple phototrophic bacteria. Springer Netherlands, pp 31-55. doi:https://doi.org/10.1007/978-1-4020-8815-5_3

  12. Tang K, Jia LJ, Yuan B, Yang SS, Li H, Meng J, Zeng Y, Feng F (2018) Aerobic Anoxygenic Phototrophic Bacteria Promote the Development of Biological Soil Crusts. Front Microbiol 9:2715. https://doi.org/10.3389/fmicb.2018.02715

    Article  PubMed  PubMed Central  Google Scholar 

  13. Li K, Liu R, Zhang H, Yun J (2013) The Diversity and Abundance of Bacteria and Oxygenic Phototrophs in Saline Biological Desert Crusts in **njiang, Northwest China. Microb Ecol 66(1):40–48. https://doi.org/10.1007/s00248-012-0164-1

    Article  CAS  PubMed  Google Scholar 

  14. Koblizek M (2015) Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol Rev 39(6):854–870. https://doi.org/10.1093/femsre/fuv032

    Article  CAS  PubMed  Google Scholar 

  15. Garcia-Chaves MC, Cottrell MT, Kirchman DL, Ruiz-Gonzalez C, Del Giorgio PA (2016) Single-cell activity of freshwater aerobic anoxygenic phototrophic bacteria and their contribution to biomass production. ISME J 10(7):1579–1588. https://doi.org/10.1038/ismej.2015.242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jiang HC, Dong HL, Yu BS, Lv G, Deng SC, Wu YJ, Dai MG, Jiao NZ (2009) Abundance and diversity of aerobic anoxygenic phototrophic bacteria in saline lakes on the Tibetan plateau. FEMS Microbiol Ecol 67(2):268–278. https://doi.org/10.1111/j.1574-6941.2008.00616.x

    Article  CAS  PubMed  Google Scholar 

  17. Hamilton TL, Bennett AC, Murugapiran SK, Havig JR (2019). mSystems 4(6):e00498–e00419. https://doi.org/10.1128/mSystems.00498-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ferrera I, Sarmento H, Priscu JC, Chiuchiolo A, Gonzalez JM, Grossart HP (2017) Diversity and Distribution of Freshwater Aerobic Anoxygenic Phototrophic Bacteria across a Wide Latitudinal Gradient. Front Microbiol 8:175. https://doi.org/10.3389/fmicb.2017.00175

    Article  PubMed  PubMed Central  Google Scholar 

  19. Zhang K, Shi Y, Cui X, Yue P, Li K, Liu X, Tripathi BM, Chu H (2019). mSystems 4(1):e00225–e00218. https://doi.org/10.1128/mSystems.00225-18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Csotonyi JT, Swiderski J, Stackebrandt E, Yurkov V (2010) A new environment for aerobic anoxygenic phototrophic bacteria: biological soil crusts. Environ Microbiol Rep 2(5):651–656. https://doi.org/10.1111/j.1758-2229.2010.00151.x

    Article  CAS  PubMed  Google Scholar 

  21. Tahon G, Willems A (2017) Isolation and characterization of aerobic anoxygenic phototrophs from exposed soils from the Sør Rondane Mountains, East Antarctica. Syst Appl Microbiol 40(6):357–369. https://doi.org/10.1016/j.syapm.2017.05.007

    Article  CAS  PubMed  Google Scholar 

  22. da Rocha UN, Cadillo-Quiroz H, Karaoz U, Rajeev L, Klitgord N, Dunn S, Truong V, Buenrostro M, Bowen BP, Garcia-Pichel F, Mukhopadhyay A, Northen TR, Brodie EL (2015) Isolation of a significant fraction of non-phototroph diversity from a desert Biological Soil Crust. Front Microbiol 6:277. https://doi.org/10.3389/fmicb.2015.00277

    Article  Google Scholar 

  23. Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22(11):569–574. https://doi.org/10.1016/j.tree.2007.09.006

    Article  Google Scholar 

  24. Van der Rest M, Gingras G (1974) The Pigment Complement of the Photosynthetic Reaction Center Isolated from Rhodospirillum rubrum. J Biol Chem 249(20):6446–6453. https://doi.org/10.1016/S0021-9258(19)42177-7

    Article  PubMed  Google Scholar 

  25. **ong JB, Sun HB, Peng F, Zhang HY, Xue X, Gibbons SM, Gilbert JA, Chu HY (2014) Characterizing changes in soil bacterial community structure in response to short-term warming. FEMS Microbiol Ecol 89(2):281–292. https://doi.org/10.1111/1574-6941.12289

    Article  CAS  PubMed  Google Scholar 

  26. Zhou XB, Tao Y, Yin BF, Tucker C, Zhang YM (2020) Nitrogen pools in soil covered by biological soil crusts of different successional stages in a temperate desert in Central Asia. Geoderma 366:114166. https://doi.org/10.1016/j.geoderma.2019.114166

    Article  CAS  Google Scholar 

  27. Zhou W, Jiang X, Ouyang J, Lu B, Liu W, Liu G (2020) Environmental Factors, More Than Spatial Distance, Explain Community Structure of Soil Ammonia-Oxidizers in Wetlands on the Qinghai–Tibetan Plateau. Microorganisms 8(6):933. https://doi.org/10.3390/microorganisms8060933

    Article  CAS  PubMed Central  Google Scholar 

  28. Mingorance MD, Barahona E, Fernandez-Galvez J (2007) Guidelines for improving organic carbon recovery by the wet oxidation method. Chemosphere 68(3):409–413. https://doi.org/10.1016/j.chemosphere.2007.01.021

    Article  CAS  PubMed  Google Scholar 

  29. 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(3):418–428. https://doi.org/10.1111/j.1574-6941.2010.00854.x

    Article  CAS  PubMed  Google Scholar 

  30. Yutin N, Suzuki MT, Beja O (2005) Novel Primers Reveal Wider Diversity among Marine Aerobic Anoxygenic Phototrophs. Appl Environ Microbiol 71(12):8958–8962. https://doi.org/10.1128/AEM.71.12.8958-8962.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Waidner LA, Kirchman DL (2008) Diversity and Distribution of Ecotypes of the Aerobic Anoxygenic Phototrophy Gene pufM in the Delaware Estuary. Appl Environ Microbiol 74(13):4012–4021. https://doi.org/10.1128/AEM.02324-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Keck F, Millet L, Debroas D, Etienne D, Galop D, Rius D, Domaizon I (2020) Assessing the response of micro-eukaryotic diversity to the Great Acceleration using lake sedimentary DNA. Nat Commun 11(1):3831. https://doi.org/10.1038/s41467-020-17682-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Luo ZM, Liu JX, Zhao PY, Jia T, Li C, Chai BF (2019) Biogeographic Patterns and Assembly Mechanisms of Bacterial Communities Differ Between Habitat Generalists and Specialists Across Elevational Gradients. Front Microbiol 10:169. https://doi.org/10.3389/fmicb.2019.00169

    Article  PubMed  PubMed Central  Google Scholar 

  34. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O’Hara RB, Simpson G, Solymos P, Stevens MHH, Wagner H (2016) Vegan: Community Ecology Package, R package version 2.3-5. https://cran.r-project.org/src/contrib/Archive/vegan/

  35. Shannon CE (1948) A Mathematical Theory of Communication. Bell Syst Tech J 27(3):379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x

    Article  Google Scholar 

  36. Chao A, Shen TJ (2003). Environ Ecol Stat 10(4):429–443. https://doi.org/10.1023/A:1026096204727

    Article  Google Scholar 

  37. Simpson EH (1949) Measurement of Diversity. Nature 163(4148):688–688. https://doi.org/10.1038/163688a0

    Article  Google Scholar 

  38. 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(2):430–440. https://doi.org/10.1038/ismej.2013.146

    Article  CAS  PubMed  Google Scholar 

  39. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) VARIATION PARTITIONING OF SPECIES DATA MATRICES: ESTIMATION AND COMPARISON OF FRACTIONS. Ecology 87(10):2614–2625. https://doi.org/10.1890/0012-9658(2006)87[2614:vposdm]2.0.co;2

    Article  PubMed  Google Scholar 

  40. McArdle BH, Anderson MJ (2001) FITTING MULTIVARIATE MODELS TO COMMUNITY DATA: A COMMENT ON DISTANCE-BASED REDUNDANCY ANALYSIS. Ecology 82(1):290–297. https://doi.org/10.1890/0012-9658(2001)082[0290:Fmmtcd]2.0.Co;2

    Article  Google Scholar 

  41. De'ath G (2001) Multivariate Regression Trees: A New Technique for Modeling Species-Environment Relationships. Ecology 83:1105–1117. https://doi.org/10.2307/3071917

    Article  Google Scholar 

  42. Praeg N, Seeber J, Leitinger G, Tasser E, Newesely C, Tappeiner U, Illmer P (2020) The role of land management and elevation in sha** soil microbial communities: Insights from the Central European Alps. Soil Biol Biochem 150:107951. https://doi.org/10.1016/j.soilbio.2020.107951

    Article  CAS  Google Scholar 

  43. Wickham H (2009) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. https://doi.org/10.1007/978-0-387-98141-3

  44. Shao JL, Lai B, Jiang W, Wang JT, Hong YH, Chen FB, Tan SQ, Guo LX (2019) Diversity and Co-Occurrence Patterns of Soil Bacterial and Fungal Communities of Chinese Cordyceps Habitats at Shergyla Mountain, Tibet: Implications for the Occurrence. Microorganisms 7(9):284. https://doi.org/10.3390/microorganisms7090284

    Article  CAS  PubMed Central  Google Scholar 

  45. Rui J, Li J, Wang S, An J, Liu W-T, Lin Q, Yang Y, He Z, Li X (2015). Appl Environ Microbiol 81(17):6070. https://doi.org/10.1128/AEM.00557-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Velasco Ayuso S, Onatibia GR, Maestre FT, Yahdjian L (2020) Grazing pressure interacts with aridity to determine the development and diversity of biological soil crusts in Patagonian rangelands. Land Degrad Dev 31(4):488–499. https://doi.org/10.1002/ldr.3465

    Article  Google Scholar 

  47. Hou J, Wu L, Liu W, Ge Y, Mu T, Zhou T, Li Z, Zhou J, Sun X, Luo Y, Christie P (2020) Biogeography and diversity patterns of abundant and rare bacterial communities in rice paddy soils across China. Sci Total Environ 730:139116. https://doi.org/10.1016/j.scitotenv.2020.139116

    Article  CAS  PubMed  Google Scholar 

  48. Angel R, Conrad R (2013) Elucidating the microbial resuscitation cascade in biological soil crusts following a simulated rain event. Environ Microbiol 15(10):2799–2815. https://doi.org/10.1111/1462-2920.12140

    Article  CAS  PubMed  Google Scholar 

  49. Yeoh YK, Dennis PG, Paungfoo-Lonhienne C, Weber L, Brackin R, Ragan MA, Schmidt S, Hugenholtz P (2017) Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nat Commun 8(1):215. https://doi.org/10.1038/s41467-017-00262-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Biebl H, Allgaier M, Tindall BJ, Koblizek M, Lunsdorf H, Pukall R, Wagner-Dobler I (2005) Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagellates. Int J Syst Evol Microbiol 55:1089–1096. https://doi.org/10.1099/ijs.0.63511-0

    Article  CAS  PubMed  Google Scholar 

  51. Bill N, Tomasch J, Riemer A, Muller K, Kleist S, Schmidt-Hohagen K, Wagner-Dobler I, Schomburg D (2017) Fixation of CO2using the ethylmalonyl-CoA pathway in the photoheterotrophic marine bacteriumDinoroseobacter shibae. Environ Microbiol 19(7):2645–2660. https://doi.org/10.1111/1462-2920.13746

    Article  CAS  PubMed  Google Scholar 

  52. Liu W, Jiang HC, Yang J, Wu G (2018) Salinity and DOC Influence the Distribution of Free-living and Particle-attached Aerobic Anoxygenic Phototrophic Bacteria in the Qinghai–Tibetan Lakes. Geomicrobiol J 35(3):247–254. https://doi.org/10.1080/01490451.2017.1364805

    Article  CAS  Google Scholar 

  53. Evans RD, Lange OL (2001) In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Ecological Studies. Springer, Berlin, pp 263–279. https://doi.org/10.1007/978-3-642-56475-8_20

    Chapter  Google Scholar 

  54. Flechtner VR, Johansen JR, Clark WH (1998). Great Basin Nat 58(4):295–311

    Google Scholar 

  55. Pitschmann H (1963) Vorarbeiten zu einer monographie der gattung Heterococcus. Nova Hedwgia 5:487–531

    Google Scholar 

  56. Hollister EB, Engledow AS, Hammett AJM, Provin TL, Wilkinson HH, Gentry TJ (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4(6):829–838. https://doi.org/10.1038/ismej.2010.3

    Article  CAS  PubMed  Google Scholar 

  57. Ben-Amotz A, Avron M (1973) The Role of Glycerol in the Osmotic Regulation of the Halophilic AlgaDunaliella parva. Plant Physiol 51(5):875–878. https://doi.org/10.1104/pp.51.5.875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Abed RMM, Tamm A, Hassenruck C, Al-Rawahi AN, Rodriguez-Caballero E, Fiedler S, Maier S, Weber B (2019) Habitat-dependent composition of bacterial and fungal communities in biological soil crusts from Oman. Sci Rep 9(1):6468. https://doi.org/10.1038/s41598-019-42911-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Masin M, Cuperova Z, Hojerova E, Salka I, Grossart HP, Koblizek M (2012) Distribution of aerobic anoxygenic phototrophic bacteria in glacial lakes of northern Europe. Aquat Microb Ecol 66(1):77–86. https://doi.org/10.3354/ame01558

    Article  Google Scholar 

  60. Bibiloni-Isaksson J, Seymour JR, Ingleton T, van de Kamp JV, Bodrossy L, Brown MV (2016) Spatial and temporal variability of aerobic anoxygenic photoheterotrophic bacteria along the east coast of Australia. Environ Microbiol 18(12):4485–4500. https://doi.org/10.1111/1462-2920.13436

    Article  CAS  PubMed  Google Scholar 

  61. Rath KM, Rousk J (2015) Salt effects on the soil microbial decomposer community and their role in organic carbon cycling: A review. Soil Biol Biochem 81:108–123. https://doi.org/10.1016/j.soilbio.2014.11.001

    Article  CAS  Google Scholar 

  62. Kopejtka K, Tomasch J, Zeng YH, Tichy M, Sorokin DY, Koblizek M (2017) Genomic Analysis of the Evolution of Phototrophy among Haloalkaliphilic Rhodobacterales. Genome Biol Evol 9(7):1950–1962. https://doi.org/10.1093/gbe/evx141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Drews G (1981) Rhodospirillum salexigens, spec. nov., an obligatory halophilic phototrophic bacterium. Arch Microbiol 130(4):325–327. https://doi.org/10.1007/BF00425949

    Article  CAS  Google Scholar 

  64. Zhu D, Han R, Long Q, Gao X, **ng J, Shen G, Li Y, Wang R (2020) An evaluation of the core bacterial communities associated with hypersaline environments in the Qaidam Basin, China. Arch Microbiol 202(8):2093–2103. https://doi.org/10.1007/s00203-020-01927-7

    Article  CAS  PubMed  Google Scholar 

  65. Cytryn EJ, Sangurdekar DP, Streeter JG, Franck WL, Chang WS, Stacey G, Emerich DW, Joshi T, Xu D, Sadowsky MJ (2007) Transcriptional and Physiological Responses of Bradyrhizobium japonicum to Desiccation-Induced Stress. J Bacteriol 189(19):6751–6762. https://doi.org/10.1128/JB.00533-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Seneviratne G, Indrasena IK (2006) Nitrogen fixation in lichens is important for improved rock weathering. J Biosci 31(5):639–643. https://doi.org/10.1007/Bf02708416

    Article  PubMed  Google Scholar 

  67. Maier S, Schmidt TSB, Zheng LJ, Peer T, Wagner V, Grube M (2014) Analyses of dryland biological soil crusts highlight lichens as an important regulator of microbial communities. Biodivers Conserv 23(7):1735–1755. https://doi.org/10.1007/s10531-014-0719-1

    Article  Google Scholar 

  68. Mastrobuoni G, Irgang S, Pietzke M, Assmus HE, Wenzel M, Schulze WX, Kempa S (2012) Proteome dynamics and early salt stress response of the photosynthetic organism Chlamydomonas reinhardtii. BMC Genomics 13:215. https://doi.org/10.1186/1471-2164-13-215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Oren A (2014) The ecology of Dunaliella in high-salt environments. J Biol Res-Thessalon 21:21. https://doi.org/10.1186/s40709-014-0023-y

    Article  Google Scholar 

  70. Darling RB, Friedmann EI, Broady PA (1987) HETEROCOCCUS ENDOLITHICUS SP. NOV. (XANTHOPHYCEAE) AND OTHER TERRESTRIAL HETEROCOCCUS SPECIES FROM ANTARCTICA: MORPHOLOGICAL CHANGES DURING LIFE HISTORY AND RESPONSE TO TEMPERATURE1. J Phycol 23(4):598–607. https://doi.org/10.1111/j.1529-8817.1987.tb04212.x

    Article  CAS  PubMed  Google Scholar 

  71. Hu CX, Zhang DL, Huang ZB, Liu YD (2003) The vertical microdistribution of cyanobacteria and green algae within desert crusts and the development of the algal crusts. Plant Soil 257(1):97–111. https://doi.org/10.1023/A:1026253307432

    Article  CAS  Google Scholar 

  72. Tréguer P, Bowler C, Moriceau B, Dutkiewicz S, Gehlen M, Aumont O, Bittner L, Dugdale R, Finkel Z, Iudicone D, Jahn O, Guidi L, Lasbleiz M, Leblanc K, Levy M, Pondaven P (2018) Influence of diatom diversity on the ocean biological carbon pump. Nat Geosci 11(1):27–37. https://doi.org/10.1038/s41561-017-0028-x

    Article  CAS  Google Scholar 

  73. Coste M, Boutry S, Tison-Rosebery J, Delmas F (2009) Improvements of the Biological Diatom Index (BDI): Description and efficiency of the new version (BDI-2006). Ecol Indic 9(4):621–650. https://doi.org/10.1016/j.ecolind.2008.06.003

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Wei Lin and Wensi Zhang from the Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences for their assistance in soil sampling and would like to thank the editors and the reviewers for the valuable suggestions to improve the manuscript.

Declaration of Authors' Contribution

H.Y. and C.H. participated in the conception of the study, carried out the general design of experiments, collected and interpreted the data, and wrote the manuscript. H.Y. performed the experiments and analyzed the data. C.H. carried out critical revisions to the article for intellectual content. All authors have read and approved the final manuscript.

Funding

This work was funded by Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA17010502) and National Natural Science Foundation of China (No. 31900237).

Author information

Authors and Affiliations

  1. Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Haijian Yang & Chunxiang Hu

Authors
  1. Haijian Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunxiang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chunxiang Hu.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Conflict of Interest

The authors declare no conflict of interest.

Supplementary Information

ESM 1

(DOCX 1580 kb)

ESM 2

(DOCX 16 kb)

ESM 3

(XLSX 64 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, H., Hu, C. Soil Chemistry and Nutrients Influence the Distribution of Aerobic Anoxygenic Phototrophic Bacteria and Eukaryotic Phototrophic Microorganisms of Physical Soil Crusts at Different Elevations on the Tibetan Plateau. Microb Ecol 83, 100–113 (2022). https://doi.org/10.1007/s00248-021-01734-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-021-01734-7

Keywords

Search

Navigation