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Ecological interactions among microbial functional guilds in the plant-soil system and implications for ecosystem function

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Felipe Albornoz at The Commonwealth Scientific and Industrial Research Organisation
Felipe Albornoz
Suzanne Prober at The Commonwealth Scientific and Industrial Research Organisation
Suzanne Prober
Megan Ryan at The University of Western Australia
Megan Ryan
Rachel J. Standish at Murdoch University
Rachel J. Standish
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Abstract and Figures

Background Soils harbour a remarkable diversity of interacting fungi, bacteria, and other microbes: together these perform a wide variety of ecological roles from nutrient cycling and organic matter breakdown, to pathogenic and symbiotic interactions with plants. Many studies demonstrate the role of microbes in plant-soil feedbacks and their interactions with plants. However, interactions among microbes are seldom addressed, and there is no consensus regarding the nature and outcomes of interactions among microbial functional guilds. Scope Here, we critically review what is known about microbe-microbe interactions among functional guilds within the plant-soil system, with the aim to initiate a path to disentangling the “microbe black-box”. Our review confirms that the nature of microbial interactions among major functional guilds is explained by niche theory. This means that, among microbes, a competitive relationship is likely when their benefits to plants, source of carbon and nutrients, or nutrient scavenging mechanisms overlap, while a neutral-to-facilitative relationship is likely when these microbial traits differ or complement each other. Conclusions We highlight the numerous knowledge gaps and provide a framework to characterise microbe-microbe interactions that offers insight into the contributions of microbes to key ecosystem functions such as carbon sequestration and nutrient cycling.
Diagram showing complexity of ecological interactions among microbial functional guilds: (A) summarises microbial interactions due to niche overlap and (B) summarises microbial interactions due to niche complementarity. The brown box represents the soil context. Blue arrows represent a facilitative interaction among microbes or between microbes and plants, while red arrows represent a negative interaction (i.e. competition or parasitism). Nitrogen (N), carbon (C), and phosphorus (P) are represented by circles. Blue arrows represent positive pathways (i.e. increase N, P, or C uptake) and interactions (i.e. facilitation), while red arrows negative pathways (i.e. N, P, or C depletion) and interactions (i.e. competition). Finally, text states the mechanism of microbe-microbe interactions: ‘resource competition 1’ refers to competition for soil P, host C, or root space; ‘resource competition 2’ refers to priority allocation of plant C to leaf endophytes over AMF; ‘resource competition 3’ refers to competition for host nutrients and C between two co-infecting pathogens or between pathogens and saprotrophs; ‘co-benefit’ refers to the complementary nutritional benefits two mutualists can offer to the same host; ‘host protection’ refers to the defence against pathogens that mutualistic microbes provide to their hosts; ‘Gadgil effect’ refers to scavenging microbes leaving behind complex C compounds that are nutritionally poor for saprotrophs; ‘priming effect’ refers to some microbes facilitating nutrient mineralization or exuding labile C compounds that are later acquired by other microbes, relieving their C constraints; ‘resource facilitation’ refers to some microbes releasing otherwise unavailable resources for other microbes; ‘co-infection’ refers to two pathogens needing to infect together; ‘interference’ refers to chemical warfare between microbes
Diagram showing complexity of ecological interactions among microbial functional guilds: (A) summarises microbial interactions due to niche overlap and (B) summarises microbial interactions due to niche complementarity. The brown box represents the soil context. Blue arrows represent a facilitative interaction among microbes or between microbes and plants, while red arrows represent a negative interaction (i.e. competition or parasitism). Nitrogen (N), carbon (C), and phosphorus (P) are represented by circles. Blue arrows represent positive pathways (i.e. increase N, P, or C uptake) and interactions (i.e. facilitation), while red arrows negative pathways (i.e. N, P, or C depletion) and interactions (i.e. competition). Finally, text states the mechanism of microbe-microbe interactions: ‘resource competition 1’ refers to competition for soil P, host C, or root space; ‘resource competition 2’ refers to priority allocation of plant C to leaf endophytes over AMF; ‘resource competition 3’ refers to competition for host nutrients and C between two co-infecting pathogens or between pathogens and saprotrophs; ‘co-benefit’ refers to the complementary nutritional benefits two mutualists can offer to the same host; ‘host protection’ refers to the defence against pathogens that mutualistic microbes provide to their hosts; ‘Gadgil effect’ refers to scavenging microbes leaving behind complex C compounds that are nutritionally poor for saprotrophs; ‘priming effect’ refers to some microbes facilitating nutrient mineralization or exuding labile C compounds that are later acquired by other microbes, relieving their C constraints; ‘resource facilitation’ refers to some microbes releasing otherwise unavailable resources for other microbes; ‘co-infection’ refers to two pathogens needing to infect together; ‘interference’ refers to chemical warfare between microbes
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https://doi.org/10.1007/s11104-022-05479-1
REVIEW ARTICLE
Ecological interactions amongmicrobial functional guilds
intheplant‑soil system andimplications forecosystem
function
FelipeE.Albornoz · SuzanneM.Prober·
MeganH.Ryan· RachelJ.Standish
Received: 24 September 2021 / Accepted: 7 May 2022
© Crown 2022
microbial interactions among major functional guilds
is explained by niche theory.This means that, among
microbes, a competitive relationship is likely when
their benefits to plants, source ofcarbon and nutrients,
or nutrient scavenging mechanisms overlap, while a
neutral-to-facilitative relationship is likelywhen these
microbial traits differ or complement each other.
Conclusions We highlight the numerous knowl-
edge gaps and provide a framework to character-
ise microbe-microbe interactions that offers insight
into thecontributions of microbes to key ecosystem
functions such as carbon sequestration and nutrient
cycling.
Keywords Ecological niche theory· Gadgil effect·
Mycorrhizal fungi· Niche complementarity· Niche
overlap· Pathogens· Saprotrophs
Abbreviations
AMF Arbuscular mycorrhizal fungi
C Carbon
DSE Dark septate endophyte
EMF Ectomycorrhizal fungi
FRE Fine root endophytes
N Nitrogen
NFB Nitrogen-fixing bacteria
P Phosphorus
PAT Plant pathogens
PSF Plant-soil feedback
SAP Soil saprotrophs
Abstract
Background Soils harbour a remarkable diver-
sity of interacting fungi, bacteria, and other
microbes: together these perform a wide variety of
ecological roles from nutrient cycling and organic
matter breakdown, topathogenic and symbiotic inter-
actions with plants. Many studies demonstrate the
role of microbes in plant-soil feedbacks and their
interactions with plants. However, interactions among
microbes are seldom addressed, andthere is no con-
sensus regarding the nature and outcomes of interac-
tions among microbial functional guilds.
Scope Here, we critically review what is known
about microbe-microbe interactions among func-
tional guilds within the plant-soil system, with the
aim to initiate a path to disentangling the “microbe
black-box”. Our review confirms that the nature of
Responsible Editor: Benjamin L. Turner.
F.E.Albornoz(*)· S.M.Prober
CSIRO Land andWater, Wembley, WA, Australia
e-mail: felipe.albornoz@csiro.au
F.E.Albornoz· M.H.Ryan
UWA School ofAgriculture andEnvironment, The
University ofWestern Australia, 35 Stirling Hwy, Crawley,
WA6009, Australia
F.E.Albornoz· R.J.Standish
Environmental andConservation Sciences, College
ofScience, Health, Engineering andEducation, Murdoch
University, 90 South Street, Murdoch, WA6150, Australia
/ Published online: 19 May 2022
Plant Soil (2022) 476:301–313
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
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