Distinct Assembly Processes and Microbial Communities Constrain Soil Organic Carbon Formation DOI Creative Commons
Mark Anthony, Thomas W. Crowther, Daniel S. Maynard

et al.

One Earth, Journal Year: 2020, Volume and Issue: 2(4), P. 349 - 360

Published: April 1, 2020

Soil stores more carbon (C) than all vegetation and the atmosphere combined. C stocks are broadly shaped by temperature, moisture, soil physical characteristics, vegetation, microbial-mediated metabolic processes. The efficiency with which microorganisms use regulates balance between storage in atmosphere. In this review, we discuss how microbial physiology community assembly processes determine growth rate and, turn, organic cycling through lens of ecology. We introduce a conceptual framework cataloging life history (i.e., rate, resource acquisition, stress tolerance) traits competition, facilitation, dispersal) that correspond different efficiencies. also compare dominant mycorrhizal fungal type affects efficiency. propose further development inclusion specific parameters microbial-explicit Earth system models needed for accurately predicting responses to global change. Globally, top two meters store ∼2,500 Pg (SOC),1Köchy M. Hiederer R. Freibauer A. Global distribution carbon—Part 1: masses frequency distributions SOC tropics, permafrost regions, wetlands, world.Soil. 2015; 351-365Crossref Scopus (107) Google Scholar whereas only holds ∼600 (C).2Ciais P. Sabine C. Bala G. Bopp L. Brovkin V. Canadell J. Chhabra DeFries Galloway Heimann et al.Carbon other biogeochemical cycles.in: Stocker T.F. Qin D. Plattner G.K. Tignor Allen S.K. Boschung Nauels Xia Y. Bex Midgley P.M. Climate Change 2013: Physical Science Basis Contribution Working Group I Fifth Assessment Report Intergovernmental Panel on Change. Cambridge University Press, 465-570Google Small changes can therefore profoundly affect atmospheric CO2 concentrations Earth's climate.2Ciais Models developed using results from soil-warming experiments predict warming will stimulate release (mostly as CO2) generate positive feedback loop could exacerbate warming.3Melillo J.M. Frey S.D. DeAngelis K.M. Werner W.J. Bernard M.J. Bowles F.P. Pold Knorr M.A. Grandy A.S. Long-term pattern magnitude climate world.Science. 2017; 358: 101-105Crossref PubMed (111) Each year, releases 60 into atmosphere, over half originates metabolism.2Ciais Scholar,4Raich J.W. Schlesinger W.H. dioxide flux respiration its relationship climate.Tellus B. 1992; 44: 81-99Crossref Total has been increasing last decades sharply indicates due is already taking place globally.5Bond-Lamberty Bailey V.L. Chen Gough C.M. Vargas Globally rising heterotrophic recent decades.Nature. 2018; 560: 80-83Crossref (63) Despite direct mediation microbes cycling, communities an overlooked component nearly major C-cycling predictions.6Sulman B.N. Moore J.A.M. Abramoff Averill Kivlin S. Georgiou K. Sridhar Hartman M.D. Wang Wieder W.R. al.Multiple underscore large uncertainty dynamics.Biogeochemistry. 141: 109-123Crossref (28) part, because represent staggering levels diversity (billions species)7Locey K.J. Lennon J.T. Scaling laws diversity.Proc. Natl. Acad. Sci. USA. 2016; 113: 5970Crossref Scholar,8Larsen B.B. Miller E.C. Rhodes M.K. Wiens J.J. Inordinate fondness multiplied redistributed: number species earth new pie life.Q. Rev. Biol. 92: 229-265Crossref (48) part lively open interdisciplinary debate.6Sulman govern matter (SOM) pools. each handful there thousands species,7Locey their death drive formation SOC.9Kallenbach Direct evidence microbial-derived ecophysiological controls.Nat. Commun. 7: 13630Crossref (228) When metabolize inputs leaf litter, rhizodeposits, amendments, or pre-existing SOC), proportion allocated growth, resulting biomass contributes (as SOM) when exuded upon cell death.10Geyer Kyker-Snowman E. Microbial efficiency: accounting population, community, ecosystem-scale controls fate metabolized matter.Biogeochemistry. 127: 173-188Crossref (81) Even though accumulates years11Li Evanylo effects long-term application amendments accumulation.Soil Water Manage. Conserv. 2013; 77: 964-973Google millennia,12Schlesinger Evidence chronosequence studies low carbon-storage potential soils.Nature. 1990; 348: 232-234Crossref (537) compounds stabilize immediate introduction13Creamer C.A. Foster A.L. Lawrence McFarland Schulz Waldrop M.P. Mineralogy dictates initial mechanism necromass association.Geochim. Cosmochim. Acta. 2019; 260: 161-176Crossref (0) advance sequestration.9Kallenbach Scholar,14Kravchenko A.N. Guber A.K. Razavi B.S. Koestel Quigely M.Y. Robertson G.P. Kuzyakov spatial footprint driver stabilization.Nat. 10: 3121Crossref (8) Since most SOM form small, charged compounds, it adsorbs active sites clays metal precipitates.15Jilling Keiluweit Contosta A.R. Schimel Schnecker Smith R.G. Tiemann Minerals rhizosphere: mediators nitrogen availability plants microbes.Biogeochemistry. 139: 103-122Crossref (27) Scholar,16Liang Amelung W. Lehmann Kästner Quantitative assessment contribution matter.Glob. 25: 3578-3590Crossref (5) These organo-mineral complexes remain bound millennia thus critical sequestration.17Lal Negassa Lorenz Carbon sequestration soil.Curr. Opin. Environ. Sustain. 15: 79-86Crossref (90) Rate key cycle, but regulated composition. Environmental filters including temperature precipitation,18Miyamoto Terashima Nara Temperature niche position breadth ectomycorrhizal fungi: reduced under predicted nested structure.Glob. 24: 5724-5737Crossref (3) physiochemical properties,19Lauber C.L. Strickland M.S. Bradford Fierer N. influence properties structure bacterial across land-use types.Soil Biochem. 2008; 40: 2407-2415Crossref (790) Scholar,20Glassman S.I. I.J. Bruns T.D. filtering pH nutrients drives fungi at fine scales.Mol. Ecol. 26: 6960-6973Crossref (50) plant communities21Van Der Linde Suz L.M. Orme C.D.L. Cox F. Andreae H. Asi Atkinson Benham Carroll Cools al.Environment host large-scale fungi.Nature. 558: 243-248Crossref (51) Scholar,22Anthony Stinson Trautwig Coates-Connor Fungal do not recover after removing invasive Alliaria petiolata (garlic mustard).Biol. Invasions. 21: 3085-3099Crossref select particular traits23Moeller H.V. Peay K.G. Fukami T. Ectomycorrhizal reflect environmental conditions along coastal California edaphic gradient.FEMS Microbiol. 2014; 87: 797-806Crossref Scholar,24Maynard D.S. Covey K.R. Lindner Glaeser Talbert D.A. Tinker P.J. Walker D.M. Crowther T.W. Consistent trade-offs trait expression broad scales.Nat. 4: 846-853Crossref (6) physiological syndromes.25Manzoni Taylor Richter Porporato Ågren G.I. stoichiometric carbon-use soils.New Phytol. 2012; 196: 79-91Crossref (477) Scholar,26Sinsabaugh R.L. Manzoni Moorhead D.L. communities: stoichiometry, methodology modelling.Ecol. Lett. 16: 930-939Crossref (274) Community composition central determinant mediate cycling. Given tremendous life, important elucidate groups regulate processes, yet our ability so remains fundamentally limited.27Wieder Kallenbach Bonan G.B. Integrating physio-chemical principles soils MIcrobial-MIneral Stabilization (MIMICS) model.Biogeosciences. 11: 3899-3917Crossref (101) Controls metabolism production frontier research.6Sulman Plant polymers resist decomposition were previously thought comprise chemical recalcitrance.28Kögel I. Estimation lignin forest humus layers.Soil 1986; 18: 589-594Crossref (199) However, advanced spectroscopy clarified adsorb minerals source SOM.16Liang Scholar,29Simpson A.J. Song Lam Novotny E.H. Hayes M.H.B. Unraveling structural components humin solution-state nuclear magnetic resonance spectroscopy.Environ. Technol. 2007; 41: 876-883Crossref (120) Functionally, referred mineral-associated matter, cycles differently larger, plant-derived particulate matter.30Lavallee Soong J.L. Cotrufo M.F. Conceptualizing forms address change 21st century.Glob. 261-273Crossref (4) slow turnover created paradigm shift research, inspired investigations understanding constraints specifically, production.25Manzoni Recent estimates suggest >50% derived exudates necromass,29Simpson some ecosystems reaches 87% Although many uncertainties must still be resolved majority characterized,31Malik A.A. Martiny J.B.H. Brodie E.L. A.C. Treseder K.K. Allison Defining trait-based strategies consequences change.ISME 14: 1-9Crossref Scholar,32Kallenbach Wallenstein Schipanksi M.E. Managing agroecosystems ecological unknowns, outcomes, path forward.Front. e1146Crossref importance contributions now well established.6Sulman ecology attempts understand underlying patterns abundances33Vellend Conceptual synthesis ecology.Q. 2010; 85: 183-206Crossref (733) help explain variation levels. varies orders lineages,34Roller B.R.K. Stoddard S.F. Schmidt T.M. Exploiting rRNA operon copy investigate reproductive strategies.Nat. e16160Crossref respire energy they (low efficiency) while others allocate (high efficiency).35Saifuddin Bhatnagar Segrè Finzi genome-scale models.Nat. 1-10Crossref (2) Scholar,36Pold Domeignoz-Horta L.A. Morrison E.W. Sistla S.A. sensitivity covary bacteria.mBio. 2020; 11https://doi.org/10.1128/mBio.02293-19Crossref accumulation biogeography, assessed molecular techniques based ribosomal DNA, clearly shown guilds organized via hierarchical processes.37Nemergut D.R. O"Neill S.P. Bilinski Stanish L.F. Knelman J.E. Darcy Lynch R.C. Wickey Ferrenberg Patterns assembly.Microbiol. Mol. 342-356Crossref (418) This suggests knowing where organisms live cycling.38Crowther van den Hoogen Wan Mayes Keiser A.D. Mo Maynard biogeochemistry.Science. 365https://doi.org/10.1126/science.aav0550Crossref (13) At same time, why provide context assembly. communities, first disperse site order establish.33Vellend Strong dispersal may selected conditions, capacity (or lack thereof) trades off certain processes.39Yawata Cordero O.X. Menolascina Hehemann J.H. Polz Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations.Proc. 111: 5622-5627Crossref (76) Scholar,40Dini-Andreote Elsas J.D. Olff Salles J.F. Dispersal-competition microbiomes quest land colonization.Sci. Rep. 8: e9451Crossref Once establish, acts against niches taxa tolerances nutrient acquisition capacities.41Vályi Mardhiah U. Rillig M.C. Hempel coexistence arbuscular fungi.ISME 2341-2351Crossref (60) Species compete facilitate establishment within communities.42Hibbing Fuqua Parsek M.R. Peterson Bacterial competition: surviving thriving jungle.Nat. 15-25Crossref investment dispersal, tolerance, competitive facilitative abilities, tradeoffs among these investments (Figure 1). synthesize life-history by-products become SOM. repository SOC, primarily throughout. insights chemistry analyses—much specific—have integrated. argue essential better merge areas research guide cohesive research. time unprecedented change, have solid basis scenarios. Fundamentally, outcome frequently represented Whole modeled incorporated versus efficiency), value ranging <0.1 >0.9 individual typically 0.25 0.8 whole depending structure, substrate type, conditions.25Manzoni Scholar,43Qiao Liang Du Z. Zhou Zhu Huang X. Luo Yan al.Global relation supply.Sci. 9: 5621Crossref What characterizes high upper range intriguing since contained substrates used does sufficient produce unit biomass.44Payne Energy yields heterotrophs.Annu. 1970; 17-52Crossref Scholar,45Roels J.A. Application macroscopic metabolism.Biotechnol. Bioeng. 1980; 22: 2457-2514Crossref Historically, constant parameter 0.55 (e.g., CENTURY46Parton Cole Ojima Analysis factors controlling grasslands Great Plains.Soil Soc. Am. 1987; 51: 1173-1179Crossref Scholar), inconsistent empirical concerning, exceptionally sensitive choice parameters.27Wieder A lower CENTURY diminishes residence consequently, sequestration.26Sinsabaugh Frameworks outlining increase decrease should occur necessary sequestration. Promising incorporate constrain (see outline Figure 1), build frameworks review include elements assembly, addition critiquing assumptions supported data. consider tolerance.27Wieder Scholar,47Chagnon P.-L. Bradley Maherali Klironomos J.N. fungi.Trends 484-491Abstract Full Text PDF Scholar, 48Malik Puissant Buckeridge Goodall Jehmlich Chowdhury Gweon H.S. Peyton Mason K.E. Agtmaal al.Land driven processes.Nat. e3591Crossref (32) 49Whitney, (2019). Physiological response availability. MSc thesis (University New Hampshire).Google basic hypothesis tolerance reduce formation. allocation toward respiration. There widespread fast efficiency.34Roller Scholar,50Novak Pfeiffer Lenski R.E. Sauer Bonhoeffer Experimental tests evolutionary trade-off yield coli.Am. Nat. 2006; 168: 242-251Crossref 51Lipson complex implications ecosystem processes.Front. 6: 615Crossref (46) 52Muscarella Trait-based approach efficiency.BioRxiv. (427161)https://doi.org/10.1101/427161Crossref Growth-rate-related Microbial-Mineral model, formation.27Wieder culture mixed growth-rate-efficiency MIMICS.34Roller Scholar,52Muscarella grow quickly ample ATP fuel efficient biosynthetic process,53Pfeiffer Evolutionary production.Z. Phys. Chem. 2002; 216: 51Crossref generally rather growth.50Novak Scholar,53Pfeiffer Fast bacteria cited overflow excess demand) reducing efficiency,25Manzoni inconsistently observed ubiquity questioned.36Pold Scholar,49Whitney, Across lines, positively correlated,36Pold Scholar,49Whit

Language: Английский

Grassland soil carbon sequestration: Current understanding, challenges, and solutions DOI
Yongfei Bai, Maurizio Cotrufo

Science, Journal Year: 2022, Volume and Issue: 377(6606), P. 603 - 608

Published: Aug. 4, 2022

Grasslands store approximately one third of the global terrestrial carbon stocks and can act as an important soil sink. Recent studies show that plant diversity increases organic (SOC) storage by elevating inputs to belowground biomass promoting microbial necromass contribution SOC storage. Climate change affects grassland modifying processes catabolism anabolism. Improved grazing management biodiversity restoration provide low-cost and/or high-carbon-gain options for natural climate solutions in grasslands. The achievable sequestration potential grasslands is 2.3 7.3 billion tons dioxide equivalents per year (CO2e year-1) restoration, 148 699 megatons CO2e year-1 improved management, 147 sown legumes pasturelands.

Language: Английский

Citations

745

Life and death in the soil microbiome: how ecological processes influence biogeochemistry DOI
Noah W. Sokol, Eric Slessarev, Gianna L. Marschmann

et al.

Nature Reviews Microbiology, Journal Year: 2022, Volume and Issue: 20(7), P. 415 - 430

Published: Feb. 28, 2022

Language: Английский

Citations

675

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements DOI Creative Commons
Grégoire T. Freschet, Loïc Pagès, Colleen M. Iversen

et al.

New Phytologist, Journal Year: 2021, Volume and Issue: 232(3), P. 973 - 1122

Published: Oct. 5, 2021

Summary In the context of a recent massive increase in research on plant root functions and their impact environment, ecologists currently face many important challenges to keep generating cutting‐edge, meaningful integrated knowledge. Consideration below‐ground components ecosystem studies has been consistently called for decades, but methodology is disparate sometimes inappropriate. This handbook, based collective effort large team experts, will improve trait comparisons across integration information databases by providing standardised methods controlled vocabularies. It meant be used not only as starting point students scientists who desire working ecosystems, also experts consolidating broadening views multiple aspects ecology. Beyond classical compilation measurement protocols, we have synthesised recommendations from literature provide key background knowledge useful for: (1) defining entities giving keys dissection, classification naming beyond fine‐root vs coarse‐root approach; (2) considering specificity produce sound laboratory field data; (3) describing typical, overlooked steps studying roots (e.g. handling, cleaning storage); (4) gathering metadata necessary interpretation results reuse. Most importantly, all traits introduced with some degree ecological that foundation understanding meaning, typical use uncertainties, methodological conceptual perspectives future research. Considering this, urge readers solely extract protocol measurements this work, take moment read reflect extensive contained broader guide ecology, including sections I–VII introductions each section description. Finally, it critical understand major aim help break down barriers between subdisciplines ecology ecophysiology, broaden researchers’ study create favourable conditions inception comprehensive experiments role functioning.

Language: Английский

Citations

405

Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits DOI Creative Commons
Shingo Miyauchi,

Enikö Kiss,

Alan Kuo

et al.

Nature Communications, Journal Year: 2020, Volume and Issue: 11(1)

Published: Oct. 12, 2020

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition terrestrial ecosystems. symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists the capacity mycorrhizal to acquire carbon from soil organic matter. Here, we present a combined analysis 135 fungal genomes 73 saprotrophic, endophytic pathogenic species, 62 including 29 new genomes. This study samples ecologically dominant guilds for which there were previously no symbiotic available, ectomycorrhizal Russulales, Thelephorales Cantharellales. Our analyses show transitions saprotrophy symbiosis involve (1) widespread losses degrading enzymes acting on lignin cellulose, (2) co-option genes saprotrophic ancestors fulfill functions, (3) diversification novel, lineage-specific symbiosis-induced genes, (4) proliferation transposable elements (5) divergent genetic innovations underlying convergent origins guild.

Language: Английский

Citations

371

Plant rhizodeposition: A key factor for soil organic matter formation in stable fractions DOI Creative Commons
Sebastián Horacio Villarino, Priscila Pinto, Robert B. Jackson

et al.

Science Advances, Journal Year: 2021, Volume and Issue: 7(16)

Published: April 14, 2021

Soil organic carbon formation remains poorly understood despite its importance for human livelihoods. Uncertainties remain the relative contributions of aboveground, root, and rhizodeposition inputs to particulate (POC) mineral-associated (MAOC) fractions. Combining a novel framework with isotope tracer studies, we quantified POC MAOC efficiencies (% C-inputs incorporated into each fraction). We found that have highest efficiency (46%) as compared roots (9%) or aboveground (7%). In addition, unexpectedly reduced formation, likely because it increased decomposition rates new POC. Conversely, root biomass (19%). Therefore, appear play opposite but complementary roles building

Language: Английский

Citations

276

Unveiling the crucial role of soil microorganisms in carbon cycling: A review DOI
Haowei Wu, Huiling Cui,

Chen-Xi Fu

et al.

The Science of The Total Environment, Journal Year: 2023, Volume and Issue: 909, P. 168627 - 168627

Published: Nov. 17, 2023

Language: Английский

Citations

204

Role of Arbuscular Mycorrhizal Fungi in Regulating Growth, Enhancing Productivity, and Potentially Influencing Ecosystems under Abiotic and Biotic Stresses DOI Creative Commons
Abdul Wahab, Murad Muhammad, Asma Munir

et al.

Plants, Journal Year: 2023, Volume and Issue: 12(17), P. 3102 - 3102

Published: Aug. 29, 2023

Arbuscular mycorrhizal fungi (AMF) form symbiotic relationships with the roots of nearly all land-dwelling plants, increasing growth and productivity, especially during abiotic stress. AMF improves plant development by improving nutrient acquisition, such as phosphorus, water, mineral uptake. tolerance resilience to stressors drought, salt, heavy metal toxicity. These benefits come from arbuscular interface, which lets fungal partners exchange nutrients, signalling molecules, protective chemical compounds. Plants' antioxidant defence systems, osmotic adjustment, hormone regulation are also affected infestation. responses promote performance, photosynthetic efficiency, biomass production in stress conditions. As a result its positive effects on soil structure, cycling, carbon sequestration, contributes maintenance resilient ecosystems. The AMFs ecological stability species- environment-specific. AMF's growth-regulating, productivity-enhancing role alleviation under is reviewed. More research needed understand molecular mechanisms that drive AMF-plant interactions their stresses. triggers plants' morphological, physiological, Water development, improved symbiosis. In colonization modulates defense mechanisms, hormonal regulation. circumstances. AMF-mediated enhanced essential oils (EOs), superoxide dismutase (SOD), peroxidase (POD), ascorbate (APX), hydrogen peroxide (H2O2), malondialdehyde (MDA), phosphorus (P). Understanding how increases adaptation reduces will help sustain agriculture, ecosystem management, climate change mitigation. have gained prominence agriculture due multifaceted roles promoting health productivity. This review delves into influences absorption, challenging environmental We further explore extent bolsters

Language: Английский

Citations

193

Mycorrhizal mycelium as a global carbon pool DOI Creative Commons
Heidi‐Jayne Hawkins,

Rachael I.M. Cargill,

Michael E. Van Nuland

et al.

Current Biology, Journal Year: 2023, Volume and Issue: 33(11), P. R560 - R573

Published: June 1, 2023

For more than 400 million years, mycorrhizal fungi and plants have formed partnerships that are crucial to the emergence functioning of global ecosystems. The importance these symbiotic for plant nutrition is well established. However, role in transporting carbon into soil systems on a scale remains under-explored. This surprising given ∼75% terrestrial stored belowground stationed at key entry point food webs. Here, we analyze nearly 200 datasets provide first quantitative estimates allocation from mycelium fungi. We estimate communities allocate 3.93 Gt CO2e per year arbuscular fungi, 9.07 ectomycorrhizal 0.12 ericoid Based this estimate, 13.12 fixed by is, least temporarily, allocated underground year, equating ∼36% current annual CO2 emissions fossil fuels. explore mechanisms which affect pools identify approaches increase our understanding fluxes via plant–fungal pathways. Our estimates, although based best available evidence, imperfect should be interpreted with caution. Nonetheless, estimations conservative, argue work confirms significant contribution made associations dynamics. findings motivate their inclusion both within climate cycling models, conservation policy practice.

Language: Английский

Citations

180

Unlocking complex soil systems as carbon sinks: multi-pool management as the key DOI Creative Commons
Gerrit Angst, Kevin E. Mueller, Michael J. Castellano

et al.

Nature Communications, Journal Year: 2023, Volume and Issue: 14(1)

Published: June 15, 2023

Much research focuses on increasing carbon storage in mineral-associated organic matter (MAOM), which may persist for centuries to millennia. However, MAOM-targeted management is insufficient because the formation pathways of persistent soil are diverse and vary with environmental conditions. Effective must also consider particulate (POM). In many soils, there potential enlarging POM pools, can over long time scales, be a direct precursor MAOM. We present framework context-dependent strategies that recognizes soils as complex systems conditions constrain MAOM formation.

Language: Английский

Citations

177

Root traits explain rhizosphere fungal community composition among temperate grassland plant species DOI Creative Commons
Christopher J. Sweeney, Franciska T. de Vries, Bart E. van Dongen

et al.

New Phytologist, Journal Year: 2020, Volume and Issue: 229(3), P. 1492 - 1507

Published: Oct. 2, 2020

Summary While it is known that interactions between plants and soil fungi drive many essential ecosystem functions, considerable uncertainty exists over the drivers of fungal community composition in rhizosphere. Here, we examined roles plant species identity, phylogeny functional traits shaping rhizosphere communities tested robustness these relationships to environmental change. We conducted a glasshouse experiment consisting 21 temperate grassland grown under three different treatments characterised within plants. found phylogenetic relatedness all affected composition. Trait with were primarily driven by arbuscular mycorrhizal fungi, root stronger predictors than leaf traits. These patterns independent under. Our results showcase key role traits, especially diameter, nitrogen specific length, driving composition, demonstrating potential for be used predictive frameworks plant–fungal relationships. Furthermore, highlight how limitations our understanding function may obscure previously unmeasured interactions.

Language: Английский

Citations

165