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

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.19560· OSTI ID:2305547
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [3]; ORCiD logo [6]; ORCiD logo [2]
  1. University of California Berkeley Berkeley CA 94720 USA, Lawrence Berkeley National Laboratory Berkeley CA 94720 USA
  2. University of California Berkeley Berkeley CA 94720 USA
  3. Lawrence Livermore National Laboratory Livermore 94550 CA USA
  4. University of California Berkeley Berkeley CA 94720 USA, Lawrence Livermore National Laboratory Livermore 94550 CA USA
  5. Lawrence Berkeley National Laboratory Berkeley CA 94720 USA
  6. Lawrence Livermore National Laboratory Livermore 94550 CA USA, University of California Merced Merced 95343 CA USA

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 intrara dices 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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); University of California, Berkeley, CA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)
Grant/Contract Number:
DE‐AC52‐07NA27344; AC02-05CH11231; AC52-07NA27344; SC0016247; SC0020163; SCW1589; SCW1678
OSTI ID:
2305547
Alternate ID(s):
OSTI ID: 2332961
Journal Information:
New Phytologist, Journal Name: New Phytologist Vol. 242 Journal Issue: 4; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (123)

Mycorrhizal Controls on Belowground Litter Quality journal September 2003
Arbuscular mycorrhiza: the mother of plant root endosymbioses journal October 2008
The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter journal February 2002
Multiple models and experiments underscore large uncertainty in soil carbon dynamics journal October 2018
The Arbuscular Mycorrhizal Fungus Funneliformis mosseae Alters Bacterial Communities in Subtropical Forest Soils during Litter Decomposition journal June 2017
Soil Microbiology and Biochemistry in Perspective book January 1989
Novel oligonucleotide primers reveal a high diversity of microbes which drive phosphorous turnover in soil journal June 2016
Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots journal April 1996
Mineral protection of soil carbon counteracted by root exudates journal March 2015
Microbial Ecology Meets Macroecology: Developing a Process‐Based Understanding of the Microbial Role in Global Ecosystems journal November 2019
Recently fixed carbon allocation in strawberry plants and concurrent inorganic nitrogen uptake through arbuscular mycorrhizal fungi journal May 2015
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? journal February 2016
The Ecology of Arbuscular Mycorrhizal Fungi journal January 2013
Bacteria Associated With a Commercial Mycorrhizal Inoculum: Community Composition and Multifunctional Activity as Assessed by Illumina Sequencing and Culture-Dependent Tools journal January 2019
Polysaccharides and monosaccharides in the hyphosphere of the arbuscular mycorrhizal fungi Glomus E3 and Glomus tenue journal February 2007
Interaction between Phosphate Solubilizing Bacteria and Arbuscular Mycorrhizal Fungi on Growth Promotion and Tuber Inulin Content of Helianthus tuberosus L journal March 2020
Organic matter quantity and source affects microbial community structure and function following volcanic eruption on Kasatochi Island, Alaska: Microbial structure and function after volcanic eruption journal July 2015
Plant-associated fungi support bacterial resilience following water limitation journal September 2022
Arbuscular Mycorrhizal Fungi Increase Organic Carbon Decomposition Under Elevated CO2 journal August 2012
Fine roots and mycorrhizal fungi accelerate leaf litter decomposition in a northern hardwood forest regardless of dominant tree mycorrhizal associations journal February 2021
Root Hairs and Plant Growth Atlow Nitrogen Availabilities journal December 1987
Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration journal December 2006
Direct evidence for the role of microbial community composition in the formation of soil organic matter composition and persistence journal November 2021
Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization journal January 2022
13C and 15N NMR spectroscopy as a tool in soil organic matter studies journal November 1997
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life journal August 2018
Mycorrhizas and soil structure journal July 2006
Trait‐based assembly of arbuscular mycorrhizal fungal communities determines soil carbon formation and retention journal May 2023
Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment: Organic nutrient uptake enhances soil C journal March 2011
An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition: AMF alters soil bacterial community and N cycling journal January 2013
Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? journal March 2019
Analysis of the community composition and bacterial diversity of the rhizosphere microbiome across different plant taxa journal November 2018
Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis journal June 2015
Quantitative Microbial Ecology through Stable Isotope Probing journal August 2015
Interactions among Glomus irregulare, arbuscular mycorrhizal spore-associated bacteria, and plant pathogens under in vitro conditions journal November 2011
Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants journal May 1990
Improved Method for Separating Light- and Heavy-Fraction Organic Material from Soil1 journal January 1987
Relative importance of sorption versus aggregation for organic matter storage in subsoil horizons of two contrasting soils journal November 2010
Soil biodiversity and soil community composition determine ecosystem multifunctionality journal March 2014
Beyond bulk: Density fractions explain heterogeneity in global soil carbon abundance and persistence journal December 2021
Mineral control of soil organic carbon storage and turnover journal September 1997
The soil matrix increases microbial C stabilization in temperate and tropical forest soils journal September 2014
Persistence of soil organic carbon caused by functional complexity journal July 2020
Model behavior of arbuscular mycorrhizal fungi: predicting soil carbon dynamics under climate change journal June 2016
Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure: Effects of AM mycelial exudates on soil bacteria journal August 2007
Microbial communities and their relevance for ecosystem models: Decomposition as a case study journal April 2010
A new fungal phylum, the Glomeromycota: phylogeny and evolution journal December 2001
Mycorrhizal Hyphal Turnover as a Dominant Process for Carbon Input into Soil Organic Matter journal March 2006
Distinct Assembly Processes and Microbial Communities Constrain Soil Organic Carbon Formation journal April 2020
Mycorrhizal Fungi as Mediators of Soil Organic Matter Dynamics journal November 2019
Mineral–Organic Associations: Formation, Properties, and Relevance in Soil Environments book December 2014
A beneficial role of arbuscular mycorrhizal fungi in influencing the effects of silver nanoparticles on plant-microbe systems in a soil matrix journal January 2020
Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling journal May 2015
The Role of Arbuscular Mycorrhiza Fungi in the Decomposition of Fresh Residue and Soil Organic Carbon: A Mini‐Review journal May 2019
Impact of Introduction of Arbuscular Mycorrhizal Fungi on the Root Microbial Community in Agricultural Fields journal January 2019
Arbuscular mycorrhizae and terrestrial ecosystem processes journal August 2004
Microbial community response to addition of polylactate compounds to stimulate hexavalent chromium reduction in groundwater journal October 2011
The fungal–mineral interface: challenges and considerations of micro-analytical developments journal November 2009
Bamboo forest expansion increases soil organic carbon through its effect on soil arbuscular mycorrhizal fungal community and abundance journal September 2017
Global mycorrhizal plant distribution linked to terrestrial carbon stocks journal November 2019
Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralisation journal May 2016
Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization journal August 2009
Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species journal January 2006
Mycorrhizal ecology and evolution: the past, the present, and the future journal February 2015
Arbuscular mycorrhizal fungi inoculation mediated changes in rhizosphere bacterial community structure while promoting revegetation in a semiarid ecosystem journal April 2017
Ultrastructural Characterization of the Lower Motor System in a Mouse Model of Krabbe Disease journal December 2016
Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways journal February 2021
Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing journal February 2011
The Composition and Phosphorus Cycling Potential of Bacterial Communities Associated With Hyphae of Penicillium in Soil Are Strongly Affected by Soil Origin journal January 2020
Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae journal January 2021
Metabolite profiling of the hyphal exudates of Rhizophagus clarus and Rhizophagus irregularis under phosphorus deficiency journal January 2021
Glomalin – Truths, myths, and the future of this elusive soil glycoprotein journal February 2021
Belowground allocation and dynamics of recently fixed plant carbon in a California annual grassland journal February 2022
Mycorrhizal Fungi Influence Soil Structure book January 2000
Mycorrhizal mycelium as a global carbon pool journal June 2023
Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition journal January 2012
NanoSIP: NanoSIMS Applications for Microbial Biology book January 2012
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? journal February 2013
Rice (Oryza sativa L.) nutrient management using mycorrhizal fungi and endophytic Herbaspirillum seropedicae journal June 2016
Microbial necromass under global change and implications for soil organic matter journal March 2023
Transfer of litter-derived N to soil mineral–organic associations: Evidence from decadal 15N tracer experiments journal January 2012
Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls journal November 2016
Release of acid phosphatase from extraradical hyphae of arbuscular mycorrhizal fungusRhizophagus clarus journal January 2015
Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi: PCR primers for arbuscular mycorrhizal fungi journal August 2008
Global distribution, formation and fate of mineral‐associated soil organic matter under a changing climate: A trait‐based perspective journal March 2022
Bradford reactive soil protein in Appalachian soils: distribution and response to incubation, extraction reagent and tannins journal August 2006
Estimating taxon‐specific population dynamics in diverse microbial communities journal January 2018
Persistence of soil organic matter as an ecosystem property journal October 2011
External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L.. 1. Spread of hyphae and phosphorus inflow into roots journal March 1992
Effects of forest harvest and fertiliser amendment on soil biodiversity and function can persist for decades journal August 2019
Isolation and identification of soil bacteria growing at the expense of arbuscular mycorrhizal fungi journal January 2011
Dynamic Stability of Soil Carbon: Reassessing the “Permanence” of Soil Carbon Sequestration journal November 2020
The origin of land plants: A matter of mycotrophism journal March 1975
Organic C and N stabilization in a forest soil: Evidence from sequential density fractionation journal November 2006
Routes to roots: direct evidence of water transport by arbuscular mycorrhizal fungi to host plants journal July 2022
Contribution of the arbuscular mycorrhizal symbiosis to the regulation of radial root water transport in maize plants under water deficit journal November 2019
Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates journal July 2010
Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors journal January 2011
Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning journal August 2004
Age of soil Organic Matter and soil Respiration: Radiocarbon Constraints on Belowground c Dynamics journal April 2000
Root litter decomposition slows with soil depth journal October 2018
Using stable isotopes to explore root-microbe-mineral interactions in soil journal June 2017
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 journal July 2019
Acidobacteria Subgroups and Their Metabolic Potential for Carbon Degradation in Sugarcane Soil Amended With Vinasse and Nitrogen Fertilizers journal July 2019
A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses journal January 2009
HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi journal November 2022
Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils journal January 2001
Nano-scale investigation of the association of microbial nitrogen residues with iron (hydr)oxides in a forest soil O-horizon journal October 2012
Imaging and 3D Elemental Characterization of Intact Bacterial Spores by High-Resolution Secondary Ion Mass Spectrometry journal August 2008
The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species journal January 2002
Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field: a possible role for arbuscular mycorrhizal fungi journal March 2001
Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation journal November 2014
Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches journal April 2021
A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces journal June 2007
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms journal March 2012
A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data journal September 2016
An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material journal September 2001
The growth of external AM fungal mycelium in sand dunes and in experimental systems journal January 2000
Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function journal December 2016
Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments journal May 2009
Picante: R tools for integrating phylogenies and ecology journal April 2010
Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter journal May 2021
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014