Arbuscular mycorrhiza convey significant plant carbon to a diverse hyphosphere microbial food web and mineral-associated organic matter

New Phytol. 2024 May;242(4):1661-1675. doi: 10.1111/nph.19560. Epub 2024 Feb 15.

Abstract

Arbuscular mycorrhizal fungi (AMF) transport substantial plant carbon (C) that serves as a substrate for soil organisms, a precursor of soil organic matter (SOM), and a driver of soil microbial dynamics. Using two-chamber microcosms where an air gap isolated AMF from roots, we 13CO2-labeled Avena barbata for 6 wk and measured the C Rhizophagus intraradices transferred to SOM and hyphosphere microorganisms. NanoSIMS imaging revealed hyphae and roots had similar 13C enrichment. SOM density fractionation, 13C NMR, and IRMS showed AMF transferred 0.77 mg C g-1 of soil (increasing total C by 2% relative to non-mycorrhizal controls); 33% was found in occluded or mineral-associated pools. In the AMF hyphosphere, there was no overall change in community diversity but 36 bacterial ASVs significantly changed in relative abundance. With stable isotope probing (SIP)-enabled shotgun sequencing, we found taxa from the Solibacterales, Sphingobacteriales, Myxococcales, and Nitrososphaerales (ammonium oxidizing archaea) were highly enriched in AMF-imported 13C (> 20 atom%). Mapping sequences from 13C-SIP metagenomes to total ASVs showed at least 92 bacteria and archaea were significantly 13C-enriched. Our results illustrate the quantitative and ecological impact of hyphal C transport on the formation of potentially protective SOM pools and microbial roles in the AMF hyphosphere soil food web.

Keywords: 13C SIP; arbuscular mycorrhizal fungi; hyphosphere; plant–soil–microbe interactions; soil carbon; soil food web; soil organic matter; stable isotopes.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Avena / microbiology
  • Bacteria / classification
  • Bacteria / genetics
  • Bacteria / metabolism
  • Carbon Isotopes
  • Carbon* / metabolism
  • Food Chain
  • Hyphae
  • Minerals* / metabolism
  • Mycorrhizae* / physiology
  • Organic Chemicals / metabolism
  • Plant Roots / microbiology
  • Soil / chemistry
  • Soil Microbiology

Substances

  • Carbon
  • Minerals
  • Carbon Isotopes
  • Organic Chemicals
  • Soil