Environmental selection overturns the decay relationship of soil prokaryotic community over geographic distance across grassland biotas

Abstract

Though being fundamental to global diversity distribution, little is known about the geographic pattern of soil microorganisms across different biotas on a large scale. Here, we investigated soil prokaryotic communities from Chinese northern grasslands on a scale up to 4,000 km in both alpine and temperate biotas. Prokaryotic similarities increased over geographic distance after tipping points of 1,760 - 1,920 km, generating a significant U-shape pattern. Such pattern was likely due to decreased disparities in environmental heterogeneity over geographic distance when across biotas, supported by three lines of evidences: 1) prokaryotic similarities still decreased with the environmental distance, 2) environmental selection dominated prokaryotic assembly, and 3) short-term environmental heterogeneity followed the U-shape pattern spatially, especially attributed to dissolved nutrients. In sum, these results demonstrate that environmental selection overwhelmed the geographic 'distance' effect when across biotas, overturning the previously well-accepted geographic pattern for microbes on a large scale.

Data availability

Sequencing data has been deposited in the NCBI Sequence Read Archive under accession number: PRJNA 729210

The following data sets were generated

Article and author information

Author details

  1. Biao Zhang

    College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3102-8300
  2. Kai Xue

    College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China
    For correspondence
    xuekai@ucas.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3504-0024
  3. Shutong Zhou

    College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Kui Wang

    College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Wenjing Liu

    College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Cong Xu

    Aerospace Information Research Institute, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Lizhen Cui

    College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Linfeng Li

    College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Qinwei Ran

    College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Zongsong Wang

    College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Ronghai Hu

    College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8041-2483
  12. Yanbin Hao

    College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Xiaoyong Cui

    Key Laboratory of Adaptation and Evolution of Plateau Biota, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Yanfen Wang

    College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5666-9289

Funding

Chinese Academy of Sciences (Strategic Priority Research and Program A,20050104)

  • Yanfen Wang

National Natural Science Foundation of China (42041005)

  • Kai Xue

Ministry of Science and Technology of the People's Republic of China (The Second Tibetan Plateau Scientific Expedition and Research (STEP) program,2019QZKK0304)

  • Yanfen Wang

Chinese Academy of Sciences (Strategic Priority Research Program A,XDA1907304)

  • Yanfen Wang

Chinese Academy of Sciences (Strategic Priority Research Program B,XDB15010201)

  • Yanfen Wang

Chinese Academy of Sciences (Light of West China)

  • Kai Xue

Chinese Academy of Sciences (Sanjiangyuan National Park Joint Program,LHZX-2020-02-01)

  • Yanfen Wang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David Donoso, Escuela Politécnica Nacional, Ecuador

Version history

  1. Received: May 7, 2021
  2. Preprint posted: May 14, 2021 (view preprint)
  3. Accepted: January 21, 2022
  4. Accepted Manuscript published: January 24, 2022 (version 1)
  5. Version of Record published: February 9, 2022 (version 2)

Copyright

© 2022, Zhang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 822
    views
  • 218
    downloads
  • 5
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Biao Zhang
  2. Kai Xue
  3. Shutong Zhou
  4. Kui Wang
  5. Wenjing Liu
  6. Cong Xu
  7. Lizhen Cui
  8. Linfeng Li
  9. Qinwei Ran
  10. Zongsong Wang
  11. Ronghai Hu
  12. Yanbin Hao
  13. Xiaoyong Cui
  14. Yanfen Wang
(2022)
Environmental selection overturns the decay relationship of soil prokaryotic community over geographic distance across grassland biotas
eLife 11:e70164.
https://doi.org/10.7554/eLife.70164

Share this article

https://doi.org/10.7554/eLife.70164

Further reading

    1. Computational and Systems Biology
    2. Ecology
    Kazushi Tsutsui, Ryoya Tanaka ... Keisuke Fujii
    Research Article

    Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.