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Sep 12, 2013 - Carbon utilization, microbial biomass, and respiration in biological soil crusts in the Negev Desert. Jun Yu & Naama Glazer & Yosef Steinberger.
Biol Fertil Soils (2014) 50:285–293 DOI 10.1007/s00374-013-0856-9

ORIGINAL PAPER

Carbon utilization, microbial biomass, and respiration in biological soil crusts in the Negev Desert Jun Yu & Naama Glazer & Yosef Steinberger

Received: 20 May 2013 / Revised: 18 July 2013 / Accepted: 30 August 2013 / Published online: 12 September 2013 # Springer-Verlag Berlin Heidelberg 2013

Abstract Biological soil crusts (BSCs) and the soils directly below crusts (SDBCs) (0–5 mm) were collected in the Negev Desert (Israel) during the wet and dry seasons of 2007 and 2008, gently separated, and microbial basal respiration, microbial biomass carbon (Cmic), carbon (C) source utilization rates, and catabolic diversity were analyzed using MicroRespTM plates. The seasonal-change patterns of these parameters were similar to those of soil organic C (Corg) in the BSCs, i.e., increases were observed during the dry seasons relative to the wet seasons. Few seasonal variations in q CO2 and Cmic/Corg in the BSCs indicated that the increases in crustal organism basal respiration and C source utilization rates can be attributed to microbial propagation as a result of the increases in available C during the dry seasons. High frequency of rain events, with precipitation higher than 0.1 mm during spring, can enable crustal organisms to maintain photosynthetic activity and can facilitate microbial propagation and Corg accumulation in the BSCs. The seasonal dynamics of the four biotic parameters in the SDBCs were the opposite of those of the BSCs, and C source utilization rates and catabolic diversity were higher than in the BSCs during the wet seasons. Downward migration of exopolysaccharides, crustal organism cell contents, and intracellular solutes with water infiltration can increase C and nutrient availability and enhance microbial catabolic activities and propagation in the SDBCs. J. Yu State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110164, China J. Yu : N. Glazer : Y. Steinberger (*) The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 5290002, Israel e-mail: [email protected] Y. Steinberger e-mail: [email protected]

Keywords Cyanobacteria-dominated crusts . Catabolic diversity . Seasonal dynamics . Water regime . MicroRespTM plates

Introduction Seventy percent or more of the interspaces between sparse vegetations in arid and semiarid areas throughout the world are known to be covered by biological soil crusts (BSCs) (Belnap 1995; Belnap et al. 2004). This thin living cover, consisting of cyanobacteria, bacteria, archaea, green algae, and fungi, as well as lichens and bryophytes at latesuccession stages, is considered a biotic mantle that exhibits obvious differences in physical, chemical, and biological characteristics relative to the soils directly below crusts (SDBCs) or those without BSCs (Garcia-Pichel and Belnap 1996; Castillo-Monroy et al. 2011). From a soil physical perspective, high silt and clay content (ca. 20–40 %) in the BSCs resulting from aeolian deposition entrapment can prevent wind and/or water erosion in arid and semiarid regions (Eldridge and Greene 1994; Karnieli 1997) and increase water-holding capacity of BSCs. The swelling of fine particles and cyanobacterial filamentous sheaths upon wetting may decrease crust pore size and, subsequently, have a negative effect on water infiltration rate and evaporation loss and a positive effect on runoff generation (Verrecchia et al. 1995; Kidron and Yair 1997; Veste et al. 2001). Indeed, the influence of BSCs on water movement is the result of the combined effects of a series of factors including soil texture, rainfall intensity, soil moisture status, and microbial composition and a successional stage of BSCs (Rossi et al. 2012). However, Rossi et al. (2012) demonstrated that extracellular polysaccharides excreted by crustal organisms (e.g., cyanobacteria) can significantly enhance hydraulic conductivity regardless of soil texture and crustal microbial composition

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due to increases in the number of micropores known as viable waterways within BSCs. In addition to altering soil physical processes, BSCs can also improve soil fertility through aeolian deposition entrapment, carbon (C) and nitrogen (N) fixation and release, and soil nutrient maintenance (Reynolds et al. 2001; Belnap 2002; Belnap et al. 2004). Littmann (1997) reported that N input through atmospheric deposition varies from 0.5 to 2.0 kg ha−1 a−1 in the sand dunes of the northwestern Negev, Israel. However, this value is approximately 10 % of the N input derived from BSCs, which varies from 2 to 41 kg ha−1 a−1 and generally depends on crust succession stage, location, and environmental conditions, such as moisture, temperature, light, and pH (West 1990). Likewise, C inputs from BSCs can cause a 200 % increase in total organic C content of the soil surface relative to soils without BSCs (Belnap et al. 2004). Moreover, soil nutrients such as sodium, potassium, magnesium, calcium, manganese, iron, nickel, copper, and zinc can be held and concentrated in BSCs via exopolysaccharides, metal chelators, and peptide N secreted by crustal organisms (Belnap et al. 2004). These processes not only give rise to big differences in chemical characteristics between BSCs and SDBCs in a desert ecosystem but also improve soil fertility and meet the needs of associated vascular plants and microbes colonizing the surrounding soil environment (Harper and Belnap 2001; Li et al. 2002; Xu et al. 2013). Generally, microbes colonizing BSCs exhibit two characteristics, i.e., high microbial abundance/density and more specific bacterial species, in comparison to those in the SDBCs or those without BSCs (Garcia-Pichel et al. 2003). The crustal organisms can be mainly divided into two groups, autotrophs and heterotrophs, according to their metabolic characteristics. Autotrophic crustal components are believed to account for a big proportion of the BSC biomass, while the existence of heterotrophic components makes the crustal community more diverse (Bowker et al. 2010). Gundlapally and Garcia-Pichel (2006) stated that bacteria other than phototrophs make a significant contribution to both the biomass and functional properties of BSCs based on direct counts and measurements of dark respiration rates. The abundance of bacteria within the crust is comparable to, or slightly less than that in organic-rich soils, which exceeds those colonizing the SDBCs by at least one order of magnitude (Garcia-Pichel et al. 2003). Moreover, the denaturing gradient gel electrophoresis (DGGE) fingerprints reveal that most of the bacterial species colonizing BSCs differ from those in sandy soils. This is probably the result of lengthy evolutionary histories of BSCs under the particular and extreme desert environmental conditions (Garcia-Pichel et al. 2003). Although declines in species richness and biomass of microbial communities are observed in the SDBCs relative to BSCs, little information is available for us to clarify the differences in microbial catabolic diversity between the two microcosms in an arid ecosystem.

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In the Negev Desert, which receives winter rainfall for 10 to 60 days between October and April, BSCs develop, fulfill the pioneer role of colonizing the soil surface, and are exposed to a harsh xeric environment for more than 80 % of the time (Evenari et al. 1982; Zaady et al. 2000). Under such conditions, the crustal organisms should have developed ecophysiological adaptations allowing them to maintain key physiological activities by shifting between full activity, desiccation, and dormancy, with different soil–water status (Mazor et al. 1996; Kidron et al. 1999). According to Nash et al. (1977), Kidron et al. (2000), Kidron (2005), and Wertin et al. (2012), it was hypothesized that moisture conditions are the most important factors responsible for crust establishment and success in arid and semiarid ecosystems. Since there are big differences in physicochemical and biological characteristics between BSCs and the soils directly below them, as mentioned above, we hypothesize that (1) the dynamics of microbial activity and catabolic diversity in these two microcosms will exhibit different patterns and seasonal variation and (2) due to higher quantity and quality of organic carbon, as well as higher abundance and species richness of a microbial community in BSCs relative to the soils directly below them, microbial catabolic diversity will be higher in BSCs. The aim of the present study was to provide more information regarding soil-crust microbial community seasonal dynamics and its functional (catabolic) diversity in an unpredictable heterogeneous desert ecosystem while attempting to define soil moisture availability and the validity of the aforementioned hypothesis within a single habitat.

Materials and methods Study site The field study was conducted at the Avdat Farm Research Station (31°04′ N, 34°42′E) in the Negev Desert, Israel. Elevation is 610 m above sea level. The climate of this area is characterized by dry, hot summers (mean maximum, 32 °C; mean minimum, 17.7 °C—in June), and wet, cool winters (mean maximum, 14.8 °C; mean minimum, 5.4 °C—in January). The average annual rainfall at the Avdat Station is 90 mm and occurs in scattered showers between October and April. Monthly rainfall during the study period is shown in Fig. 1. An additional source of moisture at this site is dew, which can be recorded in up to 195 days a year, with an average annual precipitation of 33 mm (Kidron 2010). Total annual evaporation is at least 3,000 mm (Evenari et al. 1982). The soils are brown, shallow, and rocky; desert soils (brown lithosols) and loessial and gray desert soils (loessian serozems) are composed of 24.1 % clay, 15.9 % silt, and 60 % sand (Dan et al. 1972; Ginzburg et al. 2008). The content of total organic

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2-mm mesh. What remained in the mesh was defined as crust, while what passed through the mesh was defined as the SDBCs. After that, subsamples of the BSCs and SDBCs from each replicate were subjected to the following analyses:

Fig. 1 Number of rainy days and monthly rainfalls at the study site during the 2006/2007 and 2007/2008 rain seasons

C, total N, and CaCO3 is 0.31, 0.02–0.03, and 58.4 %, respectively, with soil pH 7.9 (Ginzburg et al. 2008). The vegetation is a mixture of perennial shrub communities with a large variety of annuals. Predominant perennials at the research site are Hammada scoparia , Zygophyllum dumosum , and Artemisia sieberi. Interspaces between these shrubs are generally covered by 1–2-mm smooth cyanobacteria-dominated crusts consisting of 25 % fine sand, 55 % silt, and 20 % clay (Zaady and Offer 2010). The main cyanobacteria species are Microcoleus vaginatus and Nostoc punctiforme , and the main fungal species are Penicillium aurantiogriseum, Penicillium chrysogenum , Ulocladium atrum , Alternaria chlamydospora, and Sporormiella australis (Grishkan et al. 2006; Zaady and Offer 2010). Methods—crust collection The soil crust samples on four (n =4) strips of 100×10 cm between shrubs were collected at the loess-plain study site 7 days after a recorded rain event during January 2007 and 2008 (mid-wet–winter season) and mid-June 2007 and 2008 (mid-dry–summer season). To enable us to consider the four locations (replicates) as independent, while the climatic conditions and soil properties were similar, the interval between two neighboring locations was at least 50 m, but sampling sites for different seasons were close to each other at the same location. Soil crust samples from each replicate were collected using a small stainless steel shovel and immediately placed in separate rigid boxes to prevent breakage and transported in an insulated box to the laboratory. At the laboratory, the BSCs and SDBCs were separated by gently sieving the samples in a

(1) Soil moisture was determined gravimetrically by drying a 3-g subsamples at 105 °C for 48 h. (2) Soil organic C (Corg) was calculated from the percentage of organic C estimated by oxidization with dichromate in the presence of H2SO4 (Rowell 1994). (3) Basal respiration, biomass (Cmic), and functional diversity of microbial communities were detected using the MicroRespTM plate (Campbell et al. 2003). The measuring procedure followed the MicroResp manual. In brief, the BSCs were ground gently by using a pestle and mortar and were then passed through a 2-mm sieve. Ten-gram subsamples of the BSCs and SDBCs were separately weighed in a 20-ml vial, and deionized water was added to adjust soil moisture content to 40 % of the water-holding capacity (WHC) (Grace et al. 2006). Tightly closed vials with subsamples were incubated in the dark at 25 °C for 72 h before measurement. Twentyfive microliters of 15 different carbon sources representing amino acids (L -arginine, γ-amino butyric acid, L -alanine, L -cysteine-HCl, L -lysine-HCl, and Nacetyl-glucosamine), aromatic carboxylic acid (3,4dihydroxybenzoic acid), carbohydrates (D -Fructose, D -galactose, D -glucose, L -arabinose, and D -trehalose), and carboxylic acids (citric acid, L -malic acid, and oxalic acid) were added to the MicroResp deep well plates. Simultaneously, 25 μl deionized water and glucose were separately added to the deep well plates for the measurement of basal respiration and biomass of soil microbial communities, according to Anderson and Domsch (1978). Subsequently, the preincubated subsamples were added to the deep well plates by using a special filling device (http://www. microresp.com/MicroRespEquipment.html; Campbell et al. 2003). Carbon dioxide was measured by dye plates—a colorimetric reaction with absorbent alkali with the ability to measure CO2 evolution. A silicone rubber gasket was used to connect the deep well plate and the detection plate, and the interconnecting holes in the gasket enabled the CO2 evolved from the deep well to enter the headspace of the detection plate (Campbell et al. 2003). The detection plates were read in a spectrophotometer at 590 nm three times: immediately before placement, after 6 h, and after 24 h. During that time, the plates were incubated in the dark at 22 °C. CO2 evolution rate was calculated according to the instructions of the manufacturer. Soil Cmic was 40.4×basal respiration+0.37 (Anderson and Domsch 1978).

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The Shannon–Weaver index (H') was used to determine microbial functional diversity (Zak et al. 1994; Berg and Steinberger 2008). Two ecophysiological indices, i.e., microbial metabolic quotient (qCO2) and microbial coefficient (Cmic/Corg), were used to reflect the responses of soil microbial communities to the changes in environmental conditions. Generally, q CO2 reflects the maintenance energy requirement of soil microbial communities, and Cmic/Corg reflects the carbon availability for the growth of soil microbes (Anderson 2003). q CO2 (mg CO2-C g−1 Cmic h−1) was (basal respiration×1,000)/Cmic (Anderson and Domsch 1985), and microbial coefficient (%) was (Cmic/Corg)×100 % (Anderson 2003). Data analysis Statistical analysis was conducted using the SAS statistical software package. General linear-model analysis was used to determine the effects of sampling season, habitat, and the interaction between the two on soil properties, activity, biomass, and catabolic diversity of microbial communities. The differences in abiotic and biotic parameters between different seasons or between different microcosms were determined using Duncan's multiple range tests or student's t test, respectively. Differences at the p 0.1 mm), the longer the photosynthetic-activity time and, subsequently, the greater the C gain in BSCs will be (Bowker et al. 2002). In the present study, 20 and 6 rain events, with each precipitation larger than 0.1 mm, were recorded during Feb and May in 2007 and 2008, respectively, thus leading to a 91.1 and 51.6 % increase in Corg in the BSCs during D1 and D2 relative to W1 and W2, respectively. Another probable reason for such great seasonal changes in Corg in the BSCs was the dilution effect that occurred during the wet seasons, especially W2, i.e., in comparison with dry seasons, more soil particles could be held onto wetter BSCs during the wet seasons, which resulted in dilution of Corg in the BSCs. In future studies, weighing of the two fractions, i.e., the BSCs and SDBCs of each 0–5-mm sample, will give us more data to gage the dilution effect and, subsequently, correctly estimate total C stocks and seasonal changes in both the BSCs and SDBCs. In addition, monitoring microbial CO2 evolution in situ, assessments of the soluble C and N contents and the relative abundance and constituents of exopolysaccharides released by crustal organisms in the two microcosms, in combination with intensive sampling such as at monthly intervals, will provide more details of the dynamics of C mic , C source utilization rates, and catabolic diversity of microbial communities colonizing the BSCs and SDBCs.

292 Acknowledgments We thank Dr. Stanislav Pen-Mouratov and Ms. Gineta Barness for technical assistance. Special thanks to Ms. Ela Gindy for preparing the figures and Ms. Sharon Victor for preparing the manuscript for publication. We also would like to thank the Editor in Chief and the three anonymous reviewers for their constructive comments and suggestions that contributed to the improvement of the quality of the manuscript.

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