Temperature and substrate controls on microbial phospholipid fatty acid composition during incubation of grassland soils contrasting in organic matter quality
Introduction
Laboratory incubation of soil or litter under controlled conditions has been used to investigate soil organic matter (SOM) decomposition and the temperature responses of microorganisms utilizing SOM (Dalias et al., 2001, Bol et al., 2003). Soil preparation procedures (such as sieving and mixing) are known to disturb the microbial community and expose fresh substrates (Petersen and Klug, 1994) while prolonged soil incubation is reported to induce substrate exhaustion and stress on microbial communities (Joergensen et al., 1990). The survival rate of soil microorganisms after disturbance or the efficiency of microbial decomposition of SOM under substrate-limited conditions is documented in only a few reports (Joergensen et al., 1990, Bossio and Scow, 1998). Furthermore, the utilization of soil or litter carbon pools is associated with different groups of microorganisms, typically resulting in microbial succession during decomposition (McMahon et al., 2005). For instance, fungal growth is found to dominate during early stages of plant residue decomposition in soil (Beare et al., 1990, Feng et al., 2007), and in the decomposition of structural materials in pine litter (Berg et al., 1998). Different Gram-staining groups of bacteria, categorized by their cell wall composition, are also found to demonstrate various substrate preferences and survival strategies in a changing environment: Gram-positive bacteria are well adapted to soils with low substrate availability and in subsoils with lower organic carbon (OC) content (Griffiths et al., 1999, Fierer et al., 2003), whilst Gram-negative bacteria are more dependent on the input of fresh organic material to create “hot spots” of decomposition in soils (Griffiths et al., 1999, Kramer and Gleixner, 2006, Potthoff et al., 2006). Although not strictly related to functional traits, the relative abundance of fungi, Gram-negative and Gram-positive bacteria is informative of the microbial community composition in soil (Zhang et al., 2005, Frey et al., 2008), and may be applied to indicate microbial community shifts during soil incubation as a result of varying degree of vulnerability to substrate constraints in soil microorganisms.
Profiles of phospholipid fatty acids (PLFAs) have been used to study microbial biomass activity and community composition in various soil environments because PLFAs are only found in viable cells and hence are characteristic biomarkers for living microorganisms (Frostegård and Bååth, 1996, Evershed et al., 2006, Webster et al., 2006). Based on their chemical structures, such as branching within the molecule or the occurrence of double bonds, various PLFAs can be used to establish the notional proportions of fungi, Gram-positive bacteria (including actinomycetes) or Gram-negative bacteria (Frostegård and Bååth, 1996). Whilst phenotypic profiling techniques (such as PLFA analysis) that determine microbial membrane composition do not distinguish between microbial species (Singh et al., 2006), they can be used to determine variations in the relative abundance of fungi, Gram-negative and Gram-positive bacteria. Shifts between these microbial groups have been reported with soil warming (Biasi et al., 2005, Frey et al., 2008) and changes in microbial carbon source (recalcitrant versus labile soil carbon) are considered to be associated with these different microbial groups (Biasi et al., 2005, Bardgett et al., 2007). Hence, it is of ecological importance to investigate the temperature and substrate controls on the fungal and bacterial PLFAs during the course of soil substrate degradation. PLFAs can also be used to assess the physiological state of soil microorganisms because bacteria are known to alter their membrane fatty acid components in response to environmental changes, and therefore PLFA composition can change with respect to an external stress (Bossio and Scow, 1998, Moore-Kucera and Dick, 2008). For example, the cyclopropane PLFA was shown to be produced once a bacterial community ran out of easily degradable, soluble carbon in unleached straw and leachate treatments (Bossio and Scow, 1998). This suggests that increasing ratios of cyclopropane PLFA-to-monoenoic precursor are potential indicators of microbial starvation (Guckert et al., 1986, Bossio and Scow, 1998). Monoenoic PLFAs have been reported to be strongly related to high concentrations of available substrates (Zelles et al., 1992, Kieft et al., 1994). A decreasing ratio of monoenoic-to-saturated PLFAs (mono/sat) is typically observed when Gram-negative bacteria are starved (Guckert et al., 1986, Kieft et al., 1994). Moreover, the ratios of cyclopropane PLFA-to-monoenoic precursor and mono/sat increase and decline with increasing growth temperatures, respectively (Suutari and Laakso, 1994) and change under environmental stresses such as water limitations and metal toxins (Dickens and Anderson, 1999, Li et al., 2007, Moore-Kucera and Dick, 2008).
We report here on a study to investigate the impact of soil incubation on microbial biomass, activity, and community composition as determined by PLFA analysis at elevated temperatures in two grassland soils. These soils were shown to differ in the amount of “labile” SOM and in their stage of “oxidation” in our previous study (Feng and Simpson, 2008). The objectives of this study were to examine the temporal changes in microbial biomass and activity after soil preparation and during the soil incubation, to investigate the responses of soil PLFAs to temperature increases in soils with varied SOM quality, and to assess the efficacy of using PLFA stress indicators to evaluate substrate constraints induced by temperature increases. We hypothesize that shifts in microbial community structure might occur due to varying degrees of substrate constraints induced by elevated incubation temperatures and that the microbial community might respond differently to temperature increases in soils with varying SOM composition because the microbial community structure may be more sustainable in the soil with higher amounts of “labile” substrates.
Section snippets
Soil incubation
Surface soil samples were collected from two well-drained, pristine grassland soils in western Alberta in late August of 2005. The first soil (denoted as Soil E, classified as a Black Chernozem) was sampled from the University of Alberta Ellerslie Research Station, located south of Edmonton, Alberta, and the second (Soil L, classified as a Brown Chernozem) was collected from the Agriculture and Agri-Food Canada Research Station near Lethbridge, Alberta. Both soils are rich in calcium, have a
Microbial respiration and soil carbon content
Microbial respiration rates were generally higher in Soil L than in Soil E, and r values decreased in a pseudo-exponential mode with incubation time in both soils (Fig. 1). In Soil E, r values decreased by more than 40% in the first week of incubation and then slowly decreased to 0.25–0.36 μg CO2 gsoil−1 h−1 at the end of the experiment. In comparison, r values in Soil L decreased sharply at higher temperatures (MAT + 12 °C and MAT + 20 °C) in the first week of incubation and decreased much more slowly
Soil microbial biomass and activity during soil incubation
Major changes in the biomass and activity of the decomposer community induced by soil disturbance and substrate limitation during soil incubation may bias the analysis of SOM decomposition (Schimel and Weintraub, 2003) which is commonly investigated in soil incubation studies. Sieving and homogenization of soil samples are known to release a pool of substrates from disturbed soil and to disrupt the soil microbial community (Hassink, 1992, Petersen and Klug, 1994). Such procedures are often
Acknowledgements
We sincerely thank two anonymous reviewers for their insightful comments which greatly improved the manuscript. We thank Dr. Henry Janzen for assistance with selecting and sampling Soil L. Funding from the Canadian Foundation for Climate and Atmospheric Sciences (GR-520) is gratefully acknowledged. L. Nielsen is thanked for conducting part of the chemical extractions. The Natural Sciences and Engineering Research Council (NSERC) of Canada is thanked for support via a University Faculty Award
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