Emergent properties of microbial activity in heterogeneous soil microenvironments: Different research approaches are slowly converging, yet major challenges remain

Philippe C. Baveye, Wilfred Otten, Alexandra Kravchenko, María Balseiro-Romero, Éléonore Beckers, Maha Chalhoub, Christophe Darnault, Thilo Eickhorst, Patricia Garnier, Simona Hapca, Serkan Kiranyaz, Olivier Monga, Carsten W. Mueller, Naoise Nunan, Valérie Pot, Steffen Schlüter, Hannes Schmidt, Hans Jörg Vogel

Research output: Contribution to journalReview article

28 Citations (Scopus)
120 Downloads (Pure)

Abstract

Over the last 60 years, soil microbiologists have accumulated a wealth of experimental data showing that the bulk, macroscopic parameters (e.g., granulometry, pH, soil organic matter, and biomass contents) commonly used to characterize soils provide insufficient information to describe quantitatively the activity of soil microorganisms and some of its outcomes, like the emission of greenhouse gasses. Clearly, new, more appropriate macroscopic parameters are needed, which reflect better the spatial heterogeneity of soils at the microscale (i.e., the pore scale) that is commensurate with the habitat of many microorganisms. For a long time, spectroscopic and microscopic tools were lacking to quantify processes at that scale, but major technological advances over the last 15 years have made suitable equipment available to researchers. In this context, the objective of the present article is to review progress achieved to date in the significant research program that has ensued. This program can be rationalized as a sequence of steps, namely the quantification and modeling of the physical-, (bio)chemical-, and microbiological properties of soils, the integration of these different perspectives into a unified theory, its upscaling to the macroscopic scale, and, eventually, the development of new approaches to measure macroscopic soil characteristics. At this stage, significant progress has been achieved on the physical front, and to a lesser extent on the (bio)chemical one as well, both in terms of experiments and modeling. With regard to the microbial aspects, although a lot of work has been devoted to the modeling of bacterial and fungal activity in soils at the pore scale, the appropriateness of model assumptions cannot be readily assessed because of the scarcity of relevant experimental data. For significant progress to be made, it is crucial to make sure that research on the microbial components of soil systems does not keep lagging behind the work on the physical and (bio)chemical characteristics. Concerning the subsequent steps in the program, very little integration of the various disciplinary perspectives has occurred so far, and, as a result, researchers have not yet been able to tackle the scaling up to the macroscopic level. Many challenges, some of them daunting, remain on the path ahead. Fortunately, a number of these challenges may be resolved by brand new measuring equipment that will become commercially available in the very near future.

Original languageEnglish
Article number1929
Number of pages48
JournalFrontiers in Microbiology
Volume9
DOIs
Publication statusPublished - 27 Aug 2018

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Soil
Research
Research Personnel
Equipment and Supplies
Biomass
Ecosystem

Keywords

  • Biodiversity
  • NanoSIMS imaging
  • Single-cell genomics
  • Soil microbiology
  • Tomography
  • Upscaling
  • X-ray computed

Cite this

Baveye, Philippe C. ; Otten, Wilfred ; Kravchenko, Alexandra ; Balseiro-Romero, María ; Beckers, Éléonore ; Chalhoub, Maha ; Darnault, Christophe ; Eickhorst, Thilo ; Garnier, Patricia ; Hapca, Simona ; Kiranyaz, Serkan ; Monga, Olivier ; Mueller, Carsten W. ; Nunan, Naoise ; Pot, Valérie ; Schlüter, Steffen ; Schmidt, Hannes ; Vogel, Hans Jörg. / Emergent properties of microbial activity in heterogeneous soil microenvironments : Different research approaches are slowly converging, yet major challenges remain. In: Frontiers in Microbiology. 2018 ; Vol. 9.
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abstract = "Over the last 60 years, soil microbiologists have accumulated a wealth of experimental data showing that the bulk, macroscopic parameters (e.g., granulometry, pH, soil organic matter, and biomass contents) commonly used to characterize soils provide insufficient information to describe quantitatively the activity of soil microorganisms and some of its outcomes, like the emission of greenhouse gasses. Clearly, new, more appropriate macroscopic parameters are needed, which reflect better the spatial heterogeneity of soils at the microscale (i.e., the pore scale) that is commensurate with the habitat of many microorganisms. For a long time, spectroscopic and microscopic tools were lacking to quantify processes at that scale, but major technological advances over the last 15 years have made suitable equipment available to researchers. In this context, the objective of the present article is to review progress achieved to date in the significant research program that has ensued. This program can be rationalized as a sequence of steps, namely the quantification and modeling of the physical-, (bio)chemical-, and microbiological properties of soils, the integration of these different perspectives into a unified theory, its upscaling to the macroscopic scale, and, eventually, the development of new approaches to measure macroscopic soil characteristics. At this stage, significant progress has been achieved on the physical front, and to a lesser extent on the (bio)chemical one as well, both in terms of experiments and modeling. With regard to the microbial aspects, although a lot of work has been devoted to the modeling of bacterial and fungal activity in soils at the pore scale, the appropriateness of model assumptions cannot be readily assessed because of the scarcity of relevant experimental data. For significant progress to be made, it is crucial to make sure that research on the microbial components of soil systems does not keep lagging behind the work on the physical and (bio)chemical characteristics. Concerning the subsequent steps in the program, very little integration of the various disciplinary perspectives has occurred so far, and, as a result, researchers have not yet been able to tackle the scaling up to the macroscopic level. Many challenges, some of them daunting, remain on the path ahead. Fortunately, a number of these challenges may be resolved by brand new measuring equipment that will become commercially available in the very near future.",
keywords = "Biodiversity, NanoSIMS imaging, Single-cell genomics, Soil microbiology, Tomography, Upscaling, X-ray computed",
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Baveye, PC, Otten, W, Kravchenko, A, Balseiro-Romero, M, Beckers, É, Chalhoub, M, Darnault, C, Eickhorst, T, Garnier, P, Hapca, S, Kiranyaz, S, Monga, O, Mueller, CW, Nunan, N, Pot, V, Schlüter, S, Schmidt, H & Vogel, HJ 2018, 'Emergent properties of microbial activity in heterogeneous soil microenvironments: Different research approaches are slowly converging, yet major challenges remain', Frontiers in Microbiology, vol. 9, 1929. https://doi.org/10.3389/fmicb.2018.01929

Emergent properties of microbial activity in heterogeneous soil microenvironments : Different research approaches are slowly converging, yet major challenges remain. / Baveye, Philippe C.; Otten, Wilfred; Kravchenko, Alexandra; Balseiro-Romero, María; Beckers, Éléonore; Chalhoub, Maha; Darnault, Christophe; Eickhorst, Thilo; Garnier, Patricia; Hapca, Simona; Kiranyaz, Serkan; Monga, Olivier; Mueller, Carsten W.; Nunan, Naoise; Pot, Valérie; Schlüter, Steffen; Schmidt, Hannes; Vogel, Hans Jörg.

In: Frontiers in Microbiology, Vol. 9, 1929, 27.08.2018.

Research output: Contribution to journalReview article

TY - JOUR

T1 - Emergent properties of microbial activity in heterogeneous soil microenvironments

T2 - Different research approaches are slowly converging, yet major challenges remain

AU - Baveye, Philippe C.

AU - Otten, Wilfred

AU - Kravchenko, Alexandra

AU - Balseiro-Romero, María

AU - Beckers, Éléonore

AU - Chalhoub, Maha

AU - Darnault, Christophe

AU - Eickhorst, Thilo

AU - Garnier, Patricia

AU - Hapca, Simona

AU - Kiranyaz, Serkan

AU - Monga, Olivier

AU - Mueller, Carsten W.

AU - Nunan, Naoise

AU - Pot, Valérie

AU - Schlüter, Steffen

AU - Schmidt, Hannes

AU - Vogel, Hans Jörg

PY - 2018/8/27

Y1 - 2018/8/27

N2 - Over the last 60 years, soil microbiologists have accumulated a wealth of experimental data showing that the bulk, macroscopic parameters (e.g., granulometry, pH, soil organic matter, and biomass contents) commonly used to characterize soils provide insufficient information to describe quantitatively the activity of soil microorganisms and some of its outcomes, like the emission of greenhouse gasses. Clearly, new, more appropriate macroscopic parameters are needed, which reflect better the spatial heterogeneity of soils at the microscale (i.e., the pore scale) that is commensurate with the habitat of many microorganisms. For a long time, spectroscopic and microscopic tools were lacking to quantify processes at that scale, but major technological advances over the last 15 years have made suitable equipment available to researchers. In this context, the objective of the present article is to review progress achieved to date in the significant research program that has ensued. This program can be rationalized as a sequence of steps, namely the quantification and modeling of the physical-, (bio)chemical-, and microbiological properties of soils, the integration of these different perspectives into a unified theory, its upscaling to the macroscopic scale, and, eventually, the development of new approaches to measure macroscopic soil characteristics. At this stage, significant progress has been achieved on the physical front, and to a lesser extent on the (bio)chemical one as well, both in terms of experiments and modeling. With regard to the microbial aspects, although a lot of work has been devoted to the modeling of bacterial and fungal activity in soils at the pore scale, the appropriateness of model assumptions cannot be readily assessed because of the scarcity of relevant experimental data. For significant progress to be made, it is crucial to make sure that research on the microbial components of soil systems does not keep lagging behind the work on the physical and (bio)chemical characteristics. Concerning the subsequent steps in the program, very little integration of the various disciplinary perspectives has occurred so far, and, as a result, researchers have not yet been able to tackle the scaling up to the macroscopic level. Many challenges, some of them daunting, remain on the path ahead. Fortunately, a number of these challenges may be resolved by brand new measuring equipment that will become commercially available in the very near future.

AB - Over the last 60 years, soil microbiologists have accumulated a wealth of experimental data showing that the bulk, macroscopic parameters (e.g., granulometry, pH, soil organic matter, and biomass contents) commonly used to characterize soils provide insufficient information to describe quantitatively the activity of soil microorganisms and some of its outcomes, like the emission of greenhouse gasses. Clearly, new, more appropriate macroscopic parameters are needed, which reflect better the spatial heterogeneity of soils at the microscale (i.e., the pore scale) that is commensurate with the habitat of many microorganisms. For a long time, spectroscopic and microscopic tools were lacking to quantify processes at that scale, but major technological advances over the last 15 years have made suitable equipment available to researchers. In this context, the objective of the present article is to review progress achieved to date in the significant research program that has ensued. This program can be rationalized as a sequence of steps, namely the quantification and modeling of the physical-, (bio)chemical-, and microbiological properties of soils, the integration of these different perspectives into a unified theory, its upscaling to the macroscopic scale, and, eventually, the development of new approaches to measure macroscopic soil characteristics. At this stage, significant progress has been achieved on the physical front, and to a lesser extent on the (bio)chemical one as well, both in terms of experiments and modeling. With regard to the microbial aspects, although a lot of work has been devoted to the modeling of bacterial and fungal activity in soils at the pore scale, the appropriateness of model assumptions cannot be readily assessed because of the scarcity of relevant experimental data. For significant progress to be made, it is crucial to make sure that research on the microbial components of soil systems does not keep lagging behind the work on the physical and (bio)chemical characteristics. Concerning the subsequent steps in the program, very little integration of the various disciplinary perspectives has occurred so far, and, as a result, researchers have not yet been able to tackle the scaling up to the macroscopic level. Many challenges, some of them daunting, remain on the path ahead. Fortunately, a number of these challenges may be resolved by brand new measuring equipment that will become commercially available in the very near future.

KW - Biodiversity

KW - NanoSIMS imaging

KW - Single-cell genomics

KW - Soil microbiology

KW - Tomography

KW - Upscaling

KW - X-ray computed

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U2 - 10.3389/fmicb.2018.01929

DO - 10.3389/fmicb.2018.01929

M3 - Review article

C2 - 30210462

AN - SCOPUS:85052639442

VL - 9

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

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