Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization

Craig R See, Adrienne B Keller, Sarah E. Hobbie, Peter G Kennedy, Peter K. Weber, Jennifer Pett-Ridge

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76 Scopus citations

Abstract

Associations between soil minerals and microbially derived organic matter (often referred to as mineral-associated organic matter or MAOM) form a large pool of slowly cycling carbon (C). The rhizosphere, soil immediately adjacent to roots, is thought to control the spatial extent of MAOM formation because it is the dominant entry point of new C inputs to soil. However, emphasis on the rhizosphere implicitly assumes that microbial redistribution of C into bulk (non-rhizosphere) soils is minimal. We question this assumption, arguing that because of extensive fungal exploration and rapid hyphal turnover, fungal redistribution of soil C from the rhizosphere to bulk soil minerals is common, and encourages MAOM formation. First, we summarize published estimates of fungal hyphal length density and turnover rates and demonstrate that fungal C inputs are high throughout the rhizosphere–bulk soil continuum. Second, because colonization of hyphal surfaces is a common dispersal mechanism for soil bacteria, we argue that hyphal exploration allows for the non-random colonization of mineral surfaces by hyphae-associated taxa. Third, these bacterial communities and their fungal hosts determine the chemical form of organic matter deposited on colonized mineral surfaces. Collectively, our analysis demonstrates that omission of the hyphosphere from conceptual models of soil C flow overlooks key mechanisms for MAOM formation in bulk soils. Moving forward, there is a clear need for spatially explicit, quantitative research characterizing the environmental drivers of hyphal exploration and hyphosphere community composition across systems, as these are important controls over the rate and organic chemistry of C deposited on minerals.

Original languageEnglish (US)
Pages (from-to)2527-2540
Number of pages14
JournalGlobal change biology
Volume28
Issue number8
DOIs
StatePublished - Apr 2022

Bibliographical note

Funding Information:
We thank Luke McCormack, Chris Fernandez, Lang DeLancey, Jess Gutknecht, Peter Reich, Francois Maillard, Rachel Hestrin, and two anonymous reviewers for helpful feedback on earlier versions of this work. Christina Ramon provided invaluable assistance with the SEM and NanoSIMS imaging. Research contributing to the ideas presented here was supported by the National Science Foundation Long Term Ecological Research (LTER) program at Cedar Creek (DEB‐1831944). CS was supported by a Doctoral Dissertation Fellowship from the Graduate School of the University of Minnesota and a graduate fellowship from the U.S. Department of Energy (DOE‐SCGSR), and CS and AK were both supported by a grant from the NSF Ecosystems program (DEB‐1556529). The initial draft of this paper was written by CS during a 3‐month residency at the Sitka Center for Art and Ecology. Research conducted at Lawrence Livermore National Laboratory was supported by the Office of Biological and Environmental Research Genomic Science program as part of the Microbes Persist Soil Microbiome SFA, award SCW1632, and performed under U.S. Department of Energy Contract DE‐AC52‐07NA27344.

Funding Information:
We thank Luke McCormack, Chris Fernandez, Lang DeLancey, Jess Gutknecht, Peter Reich, Francois Maillard, Rachel Hestrin, and two anonymous reviewers for helpful feedback on earlier versions of this work. Christina Ramon provided invaluable assistance with the SEM and NanoSIMS imaging. Research contributing to the ideas presented here was supported by the National Science Foundation Long Term Ecological Research (LTER) program at Cedar Creek (DEB-1831944). CS was supported by a Doctoral Dissertation Fellowship from the Graduate School of the University of Minnesota and a graduate fellowship from the U.S. Department of Energy (DOE-SCGSR), and CS and AK were both supported by a grant from the NSF Ecosystems program (DEB-1556529). The initial draft of this paper was written by CS during a 3-month residency at the Sitka Center for Art and Ecology. Research conducted at Lawrence Livermore National Laboratory was supported by the Office of Biological and Environmental Research Genomic Science program as part of the Microbes Persist Soil Microbiome SFA, award SCW1632, and performed under U.S. Department of Energy Contract DE-AC52-07NA27344.

Publisher Copyright:
© 2022 John Wiley & Sons Ltd.

Keywords

  • MAOM
  • carbon cycling
  • carbon sequestration
  • fungal ecology
  • microbe mineral interactions

PubMed: MeSH publication types

  • Journal Article

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