Active microorganisms in soil: Critical review of estimation criteria and approaches

doi:10.1016/j.soilbio.2013.08.024

Soil Biology and Biochemistry

Volume 67, December 2013, Pages 192-211

https://doi.org/10.1016/j.soilbio.2013.08.024 Get rights and content

Highlights

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We critically evaluated literature on active soil microorganisms and revealed.
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Microorganisms in active and potentially active state: tiny versus large pool.
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Threshold parameters for microbial activity state in soil.
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Relevance of active microbial fraction in calculations of process rates.
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Combinations of dynamic approaches enable to evaluate active microbial biomass.

Abstract

Microbial functioning refers to microbial activity because only the active microorganisms drive biogeochemical processes. Despite the importance of active microorganisms, most methods focus on estimating total microbial biomass and fail to evaluate its active fraction. At first, we have described the differences among the active, potentially active, and dormant microbial states in soil and suggested threshold values of parameters for their identification. Secondly, we critically reviewed the ability of a broad range of approaches to estimate and characterize the active and the potentially active microorganisms in soil. Following approaches were evaluated: plate count and microbial cultures; direct microscopy combined with cell staining; ATP, PLFA, DNA and RNA content; microarray analyses; PCR-based approaches; stable isotope probing; soil proteomics, enzymes activity; and various approaches based on respiration and substrate utilization. The “static” approaches, mainly based on the single-stage determination of cell components (ATP, DNA, RNA, and molecular biomarkers), detect well the presence of microorganisms and total biomass, but they fail to evaluate the active part and consequently the functions. In contrast, the dynamic approaches, estimating the changes of these parameters during microbial growth and based on process rates: substrate utilization and product formation, e.g., respiration, help to evaluate active microbial biomass and relate it to specific process rates. Based on a comparison of all approaches for their universality (possibility to analyze active, potentially active and dormant microorganisms), we concluded that 1) direct microscopy with complementary stains, 2) a combination of RNA-based FISH with staining of total microbial biomass, and 3) approaches based on microbial growth were the most advantageous and allowed simultaneous quantitative estimation of active, potentially active, and dormant microorganisms in soil.

The active microorganisms compose only about 0.1–2% of the total microbial biomass and very seldom exceed 5% in soils without input of easily available substrates. Nonetheless, the fraction of potentially active microorganisms (ready to start utilization of available substrates within few hours) is much higher, contributing between 10 and 40% (up to 60%) of the total microbial biomass. Therefore, we emphasize the role of potentially active microorganisms with quick response to fluctuating substrate input in soil microhabitats and hotspots.

The transition from the potentially active to the active state occurs in minutes to hours, but the shift from dormant to active state takes anywhere from hours to days. Despite very fast activation, the reverse process – fading to the potentially active and dormant stage – requires a much longer period and is very different for individual criteria: ATP, DNA, RNA, enzyme production, respiration rates. This leads to further difficulties in the estimation of the active part of microbial community by methods based on these parameters. Consequently, the standardization, further elaboration, and broad application of approaches focused on the portion of active microorganisms in soil and their functions are urgently needed. We conclude that because active microorganisms are the solely microbial drivers of main biogeochemical processes, analyses of the active and potentially active fractions are necessary in studies focused on soil functions.

Graphical abstract

Section snippets

Introduction: why consider active microorganisms?

Studies that refer to microbial biomass are central not only in soil science but also in all biogeochemistry-related disciplines. Microbial biomass is studied not as end in itself but as a driver of biogeochemical cycles. This requires knowing which microorganisms are responsible for specific processes and, more generally, which portion of the microbial biomass is responsible for the turnover of elements.

Microbial communities in soils consist of a very broad range of organisms in different

Definitions: total, dead, dormant, and active microorganisms

The total microbial biomass includes all living and nonliving soil organisms smaller than 150–200 μm (Swift et al., 1979, Coleman and Wall, 2007). The total amount of microbial biomass is relatively small (50–2000 μg C g⁻¹ soil). It averages at 2–3% (Anderson and Domsch, 2010) and usually does not exceed 4.5% of organic C content (Anderson, 2003). The dead microorganisms are in an irreversible state in which no growth, cell elongation, or protein synthesis can take place (Villarino et al., 2000

Approaches to estimate active microorganisms in soil

We refer to the reviews of Breeuwer and Abee, 2000, Nannipieri et al., 2003, Hartmann et al., 2004, Bölter et al., 2006, Joergensen and Emmerling, 2006, Joergensen and Wichern, 2008, Musat et al., 2012 for detailed descriptions of estimation methods for microbial biomass and activity as well as their advantages and shortcomings. The present review focuses on the methods' potentials to distinguish physiological states of soil microorganisms. Several indirect criteria are often used to evaluate

Dynamics of parameters indicating changes in the physiological activity stage and microbial growth

Most of the approaches presented above showed that the portion of active microorganisms in soil is very small and is strongly dependent on the amount of easily available substrates (Fig. 3). Because the amount of available substrates in soil varies temporally and spatially by orders of magnitude, the changes of the physiological state of microorganisms are common for soil conditions. The transition of potentially active and dormant microorganisms to active state is accompanied by the sequence

Conclusions on method comparison and outlook

The importance of active microorganisms for all biogeochemical processes motivated us to prepare this review of approaches to estimate the active and potentially active parts of microbial communities. We show that despite the broad range of approaches developed to estimate the content of microbial biomass in soil, only a few have focused on its active fraction. Some of the approaches initially based on flux- or growth-related measurements (and not the content-related analyses of specific cell

Acknowledgments

We are very thankful to Prof. J.S. Waid for the invitation to prepare this review. We acknowledge long and fruitful discussions about this topic with Sergey Blagodatsky. The review was prepared because of its necessity, not because of funding. Nonetheless, the financial support of EB by DAAD, Chinese Academy of Sciences, and Russian Foundation for Basic Research (project No 12-04-01170) is strongly appreciated.

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Review paperActive microorganisms in soil: Critical review of estimation criteria and approaches

Highlights

Abstract

Graphical abstract

Section snippets

Introduction: why consider active microorganisms?

Definitions: total, dead, dormant, and active microorganisms

Approaches to estimate active microorganisms in soil

Dynamics of parameters indicating changes in the physiological activity stage and microbial growth

Conclusions on method comparison and outlook

Acknowledgments

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J. Microbiol. Methods

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Review paper
Active microorganisms in soil: Critical review of estimation criteria and approaches