Considering fungal:bacterial dominance in soils - Methods ... - CiteSeerX

Soil Biology & Biochemistry 42 (2010) 1385e1395

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Review

Considering fungal:bacterial dominance in soils e Methods, controls, and ecosystem implications Michael S. Strickland a, *,1, Johannes Rousk b, c,1 a

Forestry & Environmental Studies, Yale University, New Haven, CT 06511, USA School of the Environment and Natural Resources, Bangor University, Bangor LL57 2UW, UK c Dept. Microbial Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 December 2009 Received in revised form 7 May 2010 Accepted 11 May 2010 Available online 26 May 2010

An expectation in soil ecology is that a microbial communities’ fungal:bacterial dominance indicates both its response to environmental change and its impact on ecosystem function. We review a selection of the increasing body of literature on this subject and assess the relevance of its expectations by examining the methods used to determine, the impact of environmental factors on, and the expected ecosystem consequences of fungal:bacterial dominance. Considering methods, we observe that fungal:bacterial dominance is contingent on the actual measure used to estimate it. This has not been carefully considered; fungal:bacterial dominance of growth, biomass, and residue indicate different, and not directly relatable aspects, of the microbial community’s influence on soil functioning. Considering relationships to environmental factors, we found that shifts in fungal:bacterial dominance were not always in line with the general expectation, in many instances even being opposite to them. This is likely because the traits expected to differentiate bacteria from fungi are often not distinct. Considering the impact of fungal:bacterial dominance on ecosystem function, we similarly found that expectations were not always upheld and this too could be due to trait overlap between these two groups. We explore many of the potential reasons why expectations related to fungal:bacterial dominance were not met, highlighting areas where future research, especially furthering a basic understanding of the ecology of bacteria and fungi, is needed. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Fungal:bacterial Carbon sequestration Decomposition Carbon:nitrogen Fungi Bacteria

1. Introduction Soil microbial communities are an integral component of many ecosystem processes (Bedard and Knowles, 1989; Zak et al., 2006; Jackson et al., 2007). Because of this, the role of these communities has been studied widely (Waksman et al., 1928; Jackson et al., 2007). Although seemingly straightforward, actually gaining a detailed understanding of these communities regarding their relationship to environmental factors and ecosystem function, and developing methods to accurately assess them has often proven difficult (Barns et al., 1999). The principal contributor to these difficulties is the opaque nature of the soil environment, which makes direct observation of soil communities nearly, if not totally, impossible. Another reason is the high diversity of these communities (Torsvik et al., 2002; Fierer et al., 2007b).

* Corresponding author. Tel.: þ1 203 436 3978; fax: þ1 203 432 3929. E-mail addresses: [email protected] (M.S. Strickland), j.rousk@ bangor.ac.uk (J. Rousk). 1 Authors contributed equally to this work. 0038-0717/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2010.05.007

The dominant approach to understanding soil microbial communities has been to simplify the community by dividing it into ecologically meaningful groups (Koch, 2001). Early approaches achieved this via culturing techniques. This method provided the means of functionally classifying microorganisms by selective culturing media, for example distinguishing between cellulose degrading and lignin degrading organisms (Alexander, 1977). Another distinction made within the microbial community is based on the idea of copiotrophs versus oligotrophs where copiotrophs are organisms that thrive under high resource conditions and oligotrophs thrive under low resource conditions (Poindexter, 1981; Koch, 2001; Fierer et al., 2007a). Similar to this is Winogradsky’s idea of allochthonous versus zymogenous microbial biomass (Winogradsky, 1924) and r- versus K-selected organisms (Fontaine et al., 2003; Langer et al., 2004; Fierer et al., 2007a). Unfortunately these dichotomous definitions are either incalculable in situ or are determined post-hoc rendering them circular. One categorization of microorganisms in soil that does not suffer from many of the above shortcomings and that has been widely employed is the division between the major decomposer groups: fungi and bacteria (Waksman et al., 1928; Alexander,

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1977). It is possible that the original rationale for this separation was pragmatism derived from the early culturing techniques and subsequent staining microscopy employed to study them. Nonetheless, this general division has been maintained in soil ecology and method developments over recent decades (see Section 2.1) have enabled it to continue. This crude and potentially historically contingent approach has provided insight into soil systems leading to concepts that are widely used and discussed in soil ecology today and that are likely to increase in the future (Fig. 1). The purpose of this review is to examine recent developments with regards to distinctions made between fungal and bacterial dominance. First, in Section 2.1, we briefly discuss some current and prominent methods employed to assess fungal:bacterial dominance. In Section 2.2, we examine some of the major environmental factors that are likely to lead to differences in fungal:bacterial dominance. In Section 2.3, we discuss the relationship between fungal:bacterial dominance and two major ecosystem processes: carbon (C) sequestration and litter decomposition. Finally, we conclude by examining our current understanding of fungal: bacterial dominance and highlight areas where greater knowledge may lead to advances in this concept.

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Year Fig. 1. The prevalence of fungal:bacterial dominance in the literature today showing (A) the number of publications found using the search terms “fungal:bacterial” and “soil” and (B) the number of citations referring to those same publications from 1991 to 2008. Both works specifically related to fungal:bacterial dominance and citations of these works have increased during this period of time. In fact, extrapolating to the year 2015 suggests that articles related to fungal:bacterial dominance will increase w15 fold and citations of these articles will increase w8 fold compared to 2008 values. The number of publications and citations were identified using Web of Science. See Supplementary material for the list of articles used in this figure.

2. Review 2.1. Techniques to measure fungal:bacterial dominance Early techniques used to study soil microorganisms, primarily culture-based, will not be addressed in this review, and instead we will focus on some current and widely applied methods. An array of techniques have been developed that assess fungal:bacterial dominance (Joergensen and Wichern, 2008; Supplementary Table 1). For example, Frostegård and Bååth (1996) used phospholipid fatty acids (PLFAs) that were specific to bacteria and fungi to estimate the biomass of each group in soil. Alternatively, Anderson and Domsch (1973) used selective inhibition with fungal or bacterial specific antibiotics to similarly estimate the substrate induced respiration or SIR biomass of each group (although see Rousk et al., 2009b). Selective inhibition, PLFA techniques, ergosterol to distinguish fungi from the total microbial biomass, direct observation (i.e. microscopy), and the use of fungal/bacterial cell wall derived indicators (e.g. chitin and muramic acid) or residues, were recently reviewed by Joergensen and Wichern (2008). They found that across biomes these methods were generally comparable. However, across coarse spatial scales, different measures of whole microbial biomass are often correlated (Wardle and Ghani, 1995) which is not always true at finer scales (i.e. within one soil type). This is potentially true for estimates of fungal:bacterial dominance. Another important consideration, particularly for PLFA and ergosterol markers but other measures as well, is the potential confounding inclusion of mycorrhiza in the fungal estimate (Joergensen and Wichern, 2008; also see Section 2.2.2 where the discussion on the mycorrhizal influence on the fungal:bacterial dominance is continued). These biomarkers are also variable within the target groups that make reliable conversion factors hard to obtain. For instance, the concentration of ergosterol in fungal tissue varies between species (Joergensen, 2000; Ruzicka et al., 2000), and there are even a few fungi that lack the lipid [e.g. some Zygomycota (Weete and Gandhi, 1999)]. Methods not discussed in Joergensen and Wichern (2008) included DNA and growth-based measures. DNA-based approaches are increasingly being used to measure fungal:bacterial dominance. One approach is quantitative PCR (qPCR). It uses the accumulation of a florescent reporter molecule during the PCR reaction coupled with primers specific to either bacteria or fungi (that typically target the 16S or 18S rRNA gene segments, respectively) to determine fungal:bacterial dominance (Raeymaekers, 2000; Fierer et al., 2005). qPCR represents both a rapid and quantifiable approach to assess fungal:bacterial dominance in soils and is relatively inexpensive when compared to other molecular techniques (Fierer et al., 2005). However, caveats are associated with this technique. Foremost, is that fungal:bacterial dominance, determined via qPCR, may not indicate the abundances of these groups in soil especially on a per biomass basis. Reasons for this include the fact that fungi and bacteria differ physiologically. For instance, fungal cells may include many or no nuclei leading to an over or underestimation of fungal abundance, DNA extraction efficiencies may differ between these two groups, the amplification of genes may not be consistent across all taxa, and multiple copies of the same gene may be found within a single individual (Klappenbach et al., 2000; Martin-Laurent et al., 2001; Smith and Osborn, 2009). Additionally, because DNA is present in both active and inactive cells it may not necessarily be related to a given ecosystem process or response to environmental change (Nocker and Camper, 2009). Fungal:bacterial dominance determined via RNA based or even proteomic approaches may ultimately prove more informative when assessing relationships to environmental


change or ecosystem processes that are likely to be driven by active organisms (Poulsen et al., 1993; Aviv et al., 1996; Vestergard et al., 2008; Nocker and Camper, 2009). A set of methods distinct from biomass and DNA-based approaches, is the determination of bacterial and fungal growth. One example is the tracking of 13C signals into the DNA of the microbial community (Dumount and Murrell, 2005; Neufield et al., 2007). This is a promising approach given that it can be paired with PCR-based techniques to resolve microbial community composition, but a current lack of broad enough universal primers prevents the direct comparison of fungi and bacteria in the same analysis. Furthermore, this technique is constrained by a requirement for both high atom percent isotope enrichments and high substrate loads, in order to detect a signal (Bengtson et al., 2009). An analogous method that has proven to be sensitive and does not require high substrate loads, is the tracking of stable isotopes into fungal and bacterial PLFA biomarkers. This approach has been successful at monitoring the transfer of resources through the fungal and bacterial channels of soil food webs (Treonis et al., 2004; Olsson and Johnson, 2005; Brant et al., 2006; Williams et al., 2006). Although high substrate amounts are not required for the stable isotope e PLFA approach, one criticism is that substrates are still being introduced. This potentially alters microbial growth conditions and affects fungal:bacterial dominance. An alternative growth-based measurement is the incorporation, during short-term incubations, of trace concentrations of precursor molecules into biomass markers. For bacteria growth is generally measured as the incorporation of the precursors leucine or thymidine into macromolecules (Bååth, 1992; Bååth et al., 2001) while fungal growth is measured as acetate-in-ergosterol incorporation (Bååth, 2001). Since incubations are short the growth rate is not expected to change from the in situ rate for either group. The combination of both methods may provide a direct estimate of the relationship between fungal:bacterial dominance and a given ecosystem process or response to environmental change (Rousk and Bååth, 2007a). In fact these techniques have successfully determined the relative contribution of fungi and bacteria during decomposition (Rousk and Bååth, 2007b). However, the acetatein-ergosterol method is susceptible to the same problems that ergosterol concentration has for representing fungal biomass (see above) and a current lack of adequate conversion factors have made quantification of bacterial and fungal growth in units C difficult, although there is progress for both groups (Bååth, 1994; Rousk and Bååth, 2007b). All techniques used to determine fungal:bacterial dominance in soil are by necessity indirect and suffer from specific caveats (Supplementary Table 1). It is also likely that the interpretation of relationships between ecosystem processes/environmental change and fungal:bacterial dominance will often be dependent on the method used to determine that dominance. In short, four very different aspects of fungal:bacterial dominance have been used; (i) measurements of fungal/bacterial residues, (ii) measurements of fungal/bacterial biomass, (iii) measurements of fungal/bacterial contribution to SIR biomass, and (iv) fungal/bacterial growth rates. These different assessments of fungal:bacterial dominance will potentially produce differences in the interpretation of relationships between dominance and ecosystem processes/environmental factors. Additionally, it is unclear how different measurements can be related to each other (e.g. how growth rates can be related to biomass measures). These important aspects have not been sufficiently considered. Also, the disparate means that have been used to assess fungal:bacterial dominance and the fact that researchers often relate this ratio to a wide array of ecosystem processes and environmental factors makes a formal meta-analysis nearly impossible.

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2.2. Environmental factors affecting fungal:bacterial dominance 2.2.1. Physical disturbance and tilling effects Much of the interest in the fungal:bacterial dominance of soils, is related to agricultural practices (Hendrix et al., 1986; Holland and Coleman, 1987; Drijber et al., 2000; Bailey et al., 2002; Helgason et al., 2009). Hendrix et al. (1986) proposed that no-till agricultural practices would result in a fungal-dominated system instead of the bacterial-dominated one expected under conventional tillage practices. This expected outcome is largely based on key differences in the growth forms of fungi and bacteria (Hendrix et al., 1986). Fungi typically exhibit a hyphal growth form but most bacteria are present as individual cells. The hyphal growth form of fungi likely conveys several advantages to these organisms, chief of which is the translocation of nutrients and resources from microsites where they are abundant to sites where they are limiting (Hendrix et al., 1986; Frey et al., 2003). These advantages may be negated under conventional agricultural practices as well as other factors that physically disturb the soil [e.g. earthworms (Butenschoen et al., 2007)], even resulting in direct tissue damage to the fungi (Hendrix et al., 1986; Helgason et al., 2009). Bacteria on the other hand would be relatively unaffected by tillage since they are present as individual cells (Hendrix et al., 1986). Furthermore, tillage homogenizes the soil, evenly distributing nutrients and resources. This too negates many of the advantages conveyed to fungi (Bardgett et al., 1996, 1999; Bardgett and McAlister, 1999). Add to this the generally held idea that bacteria are more efficient colonizers of the organic resources made available post-till (e.g. newly available SOM and dead microorganisms) and the conclusion that emerges is that fungal:bacterial dominance will decrease under conventional tillage practices (Holland and Coleman, 1987). Empirical evidence in support of such impacts on fungal:bacterial dominance are as of yet far from definitive. Of five studies comparing the fungal:bacterial dominance of communities under conventional tillage practices to those under no-till practices, no consistent evidence of tillage effects were found. Of these studies, three (all using PLFA based determination of fungal:bacterial dominance) found that changes to no-till or reduced till did lead to an overall increase in microbial biomass but this increase was proportional for both bacteria and fungi (Pankhurst et al., 2002; Spedding et al., 2004; Helgason et al., 2009). Bailey et al. (2002) found that fungal dominance determined via selective inhibition increased under no-till practices but the opposite was true when fungal dominance was determined using PLFA, although this was not replicated. Fungal:bacterial dominance was determined via direct observation (staining microscopy) by Frey et al. (1999) and they found that fungal dominance did increase under no-till practices. However, closer examination of these results showed that tillage covaried with soil moisture and once this was accounted for tilling had no impact on fungal:bacterial dominance. Van Groenigen et al. (2010) assessed fungal:bacterial dominance using several different techniques and found surprisingly minor differences between conventional and reduced till treatments. They found that reduced tillage was associated with an increase in both bacterial and fungal biomass in surface soils. Also the functional dominance, determined via growth-based measures, of fungi did not increase under reduced tillage. It was concluded that reduced till could promote soil C storage due to a proportional increase in both bacterial and fungal biomass (no change in fungal:bacterial dominance) but that the functional dominance of saprotrophic fungi did not increase. This finding is consistent with previous assessments (Beare et al., 1992; Bailey et al., 2002). Although these studies question the impact that physical disturbance will have on the microbial community’s fungal:bacterial dominance, they also

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highlight that other factors may well influence the relative dominance of these two groups (e.g. soil moisture).

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2.2.2. Direct and indirect nutrient effects Another characteristic likely to influence the fungal:bacterial dominance of soil communities is nutrient availability (Bardgett and McAlister, 1999; Suzuki et al., 2009). Like physical disturbance this has been related to agricultural based management decisions such as fertilizer inputs (Bardgett et al., 1996, 1999; Bardgett and McAlister, 1999). In many ways the hypothesized impacts fertilizer inputs may have on fungal:bacterial dominance are similar to those hypothesized for tillage. For example, when fertilizer applications are broadcast, as opposed to banding or knifing, they homogenize soil nutrient availability and likely negate any advantages associated with the fungal growth form. Stoichiometric differences between bacteria and fungi are another possible reason why fungal:bacterial dominance is expected to decrease as nutrient inputs into the soil increase (van der Heijden et al., 2008). Generally the carbon:nitrogen (C:N) of bacterial biomass is expected to be w3e6 while the C:N of fungal biomass is expected to be e5e15, meaning on average fungi have a greater C:N than bacteria (McGill et al., 1981). For this reason, fungi are expected to have lower nutrient requirements and bacteria are expected to have higher requirements (Güsewell and Gessner, 2009). Subsequently, if access to C is equivalent but N is limiting then a shift toward fungal dominance is expected but if N is not limited then a shift toward bacterial dominance is expected (Hu et al., 2001; Carney et al., 2007). This rationale is not solely limited to explaining fertilizer inputs. It has also been used to explain the effects of litter quality on fungal:bacterial dominance (see Section 2.3.2 for further details) and a recent review noted a positive relationship between fungal dominance as indicated by qPCR and soil C:N ratios across biomes (Fierer et al., 2009). However, as noted by the authors, in such cross system studies it is difficult to tease out causality among many correlated factors, including soil pH, moisture, and vegetation type (and associated mycorrhiza). Much of what we know about bacterial biomass C:N can be attributed to cultured organisms. These organisms were grown on relatively nutrient rich media (McGill et al., 1981). Under these conditions bacterial nutrient composition is more constrained, while fungal nutrient composition has a wider range that correlates with the resources utilized (Sterner and Elser, 2002). However, a compilation of studies examining communities of aquatic bacteria and cultures grown on nutrient poor media shows that bacteria range in C:N from w3 to 12 (Fig. 2). Furthermore, assessments of the C:N of fungi, based largely on sporocarps [we only noted one study that determined the C:N of fungal hyphae (Wallander et al., 2003)], show a range ofe3e51 for mycorrhizal fungi ande4e60 for saprotrophic fungi (Fig. 2). This suggests the possibility that a large proportion of fungi and bacteria overlap with regards to biomass C: N (Fig. 2), although fungi appear to have the higher mean ratio. Additionally, Cleveland and Liptzin (2007) show that the C:N of total soil microbial biomass does not differ across habitats (forests to grasslands) that are expected to vary in their fungal:bacterial dominance again suggesting overlap in the biomass C:N of these groups. Admittedly though in soils less is known about the possible overlap in fungal and bacterial C:N because of difficulties in both measuring pure bacterial biomass in situ and culturing specific soil bacteria (Madsen, 2005; Kreuzer-Martin, 2007). In line with the idea that fungi and bacteria have distinct nutrient compositions, several studies have found that N fertilization impacts fungal:bacterial dominance. One example is Bardgett and McAlister (1999), who observed pastures that received little to no inputs of fertilizer N typically had a greater fungal:bacterial dominance than did sites that received large inputs. Although an

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C:N ratio Fig. 2. The distribution of the C:N ratios of bacteria, saprotrophic fungi, and mycorrhizal fungi. Shown are box plots with medians and distributions, notably fewer measurements of the C:N ratio of bacteria have been made. Results were compiled from the literature and included 1099 observations from 18 studies. Most of the data on fungi was obtained in the field from sporocarps whereas most of the data for bacteria was obtained from cultures or aquatic samples. The expected difference in the C:N ratios of fungi and bacteria is often related to both the response of these organisms to environmental change as well as how fungal:bacterial dominance may be an indicator of ecosystem processes. This figure is meant to serve as an example of how a basic understanding of these organisms might help to better predict the implications of theory related to fungal:bacterial dominance. Closed circles ¼ Mycorrhizal fungi; Open circles ¼ Saprotrophic fungi; Closed squares ¼ Bacteria. See Supplementary material for the list of articles used in this figure.

experimental component of Bardgett and McAlister’s (1999) study found that cutting date had an effect, they also found that fertilizer cessation did not lead to a significant increase in fungal:bacterial dominance after 6 years. They hypothesized that this may have been due to high residual fertility. Similar studies also report conflicting results for both pasture and forest sites (de Vries et al., 2006; Demoling et al., 2008). de Vries et al. (2006) found using a 2 year field-based experimental study that low fertilization rates led to an increase in fungal dominance (using staining microscopy). On the other hand, a follow up field observation found that fungal:bacterial dominance was not related to changes in management intensity since both bacterial and fungal biomass responded similarly to changes in management intensity (de Vries et al., 2007). Recent work by Mulder and Elser (2009) also noted that fungal:bacterial dominance (estimated using staining microscopy) decreased on average from managed (i.e. higher nutrient availability) to abandoned fields (i.e. lower nutrient availability). Högberg et al. (2003) and Demoling et al. (2008) found that across N deposition gradients in coniferous forests, fungal: bacterial dominance (estimated using PLFA) decreased as deposition increased. Interestingly however, Demoling et al. (2008) did not find a concomitant change in fungal growth (estimated using acetate-in-ergosterol incorporation) accompanying the decline in fungal biomass. The likely explanation for this was attributed to a shift toward more mycorrhizal fungi as N deposition decreased since the fungal growth estimate (i.e. acetate-in-ergosterol incorporation) is likely only relevant to saprotrophs. These findings suggest that the observed increase in mycorrhizal biomass may indicate that fungal:bacterial dominance is mediated by the type of mycorrhizae (i.e. arbuscular mycorrhizae, ectomycorrhizae, or ericoid mycorrhizae) that infect plants, a point also highlighted in the review by Joergensen and Wichern (2008). The type of mycorrhizal infection tends to be related to the overall nutrient status of the soil (Smith and Read, 1997; Lambers et al., 2008) and is also related to broad ecosystem classifications


(Treseder and Cross, 2006). For example, Treseder and Cross (2006) found that arbuscular (AM)-mycorrhizae were most abundant in temperate grasslands and least abundant in taiga systems. In taiga systems as well as acidic soils, ectomycorrhizae tend to dominate, while ericoid mycorrhizae tend to dominate in heathlands (Smith and Read, 1997). Additionally, an increase in soil nutrients have been shown to dramatically decrease the abundance of both AMmycorrhizal fungi (Oehl et al., 2004; Cruz et al., 2009; but also see Birkhofer et al., 2008) and ectomycorrhizal fungi (e.g. Nilsson et al., 2005, 2007). However, because ectomycorrhizae contain biomarkers shared by saprotrophic fungi but not present in AMmycorrhizae (including e.g. ergosterol and PLFA 18:2u6,9) there is the potential that nutrient effects on the total fungal:bacterial dominance of a community will be the outcome of fundamentally different effects in systems dominated by AM-mycorrhiza compared with systems dominated by ecto- or ericoid mycorrhiza. That is, a decline in fungal:bacterial dominance as determined with biomarkers such as ergosterol or PLFAs will be observed in an ectomycorrhizal dominated system if nutrient inputs are increased but in an AM-mycorrhizal dominated system a decline may go unnoticed (as also discussed in Joergensen and Wichern, 2008). In light of the potential, particularly for fungi, that their response to changes in nutrients may be masked, it would be advantageous when relating ecosystem processes to fungal:bacterial dominance that the distinction between fungal subgroups be made (Mayor et al., 2009; Van Groenigen et al., 2010). After all, the original reason for relating the saprotrophic fungi and bacteria is ultimately related to their similar ecological roles, which the AM and ectomycorrhiza may not share (but see Talbot et al., 2008; Baldrian, 2009 concerning the saprobic abilities of mycorrhizae). Similar arguments could of course also be made for the exclusion of certain bacterial groups. It may be necessary for researchers in the future, whenever possible, to tailor their estimates of fungal: bacterial dominance to specific fungal and bacterial subgroups in order to accurately address a research question. 2.2.3. Soil pH effects A significant impact of soil pH on the fungal:bacterial dominance of microbial communities has been shown for both forest (Blagodatskaya and Anderson, 1998; Bååth and Anderson, 2003) and arable systems (Rousk et al., 2009a). In general, fungi have been found to be more acid tolerant than bacteria leading to increased fungal dominance in acidic soils (Högberg et al., 2007; Joergensen and Wichern, 2008; Rousk et al., 2009a). However, this does not appear to be a conclusive pattern since alterations in pH can result in increased, decreased, or unchanged levels of fungal dominance (Marstorp et al., 2000; Bååth and Anderson, 2003; Högberg et al., 2007; Rousk et al., 2009a). One possibility for these variable results is that the fungalcommunity is not impacted to the same degree by pH as the bacterial community is. Work conducted across a land-use gradient in the Southeastern U.S. found the relative abundance of fungal taxa were more strongly related to soil P and C:N ratios than any other edaphic characteristic (Lauber et al., 2008). If this pattern holds true across a range of systems then it might imply that the fungi are likely to be impacted to a lesser degree than bacteria by changes in soil pH. Pureculture studies of fungi also corroborate this indicating that the pH-growth optimum for fungi is often wide, encompassing several pH units (Wheeler et al., 1991). Contrastingly, the pH optima for bacterial communities extracted from natural soils are closely constrained to the in situ conditions (Bååth, 1996), suggesting a potentially fundamental difference between the two groups. The explanation for these seemingly inconsistent pH-patterns may also be due to the inclusion of ectomycorrhizal fungi in the assessment of fungal:bacterial dominance (see also Section 2.2.2.

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for a discussion on mycorrhizae). For example, the previously observed connection between acid soils and high fungal biomass may in part be driven by increased ectomycorrhizal fungi due to a shift in plant species composition (Smith and Read, 1997; Högberg et al., 2003; Joergensen and Wichern, 2008). In a system without ectomycorrhizae and using an artificial century-old pH gradient, Rousk et al. (2009a) found that fungal growth increased more than five-fold between high and low pH (8.3 and 4.5, respectively). Conversely bacterial growth decreased in the same interval, resulting in a nearly 30-fold increase in the fungal:bacterial growth-ratio between high and low pH, confirming suggestions from earlier growth-based studies (e.g. Arao, 1999). In contrast, fungal biomass (as opposed to fungal growth) did not change with pH (Rousk et al., 2009a). That is, the concentration of fungal tissue may be largely unconnected to fungal activity, which should scale closely with the fungal growth rate in a system. This may be particularly true for fungi, where the bulk of the biomass is involved in translocation processes (i.e. does not actively interact with the surrounding soil environment) but only the hyphal tips are actively involved in decomposition and potentially actively growing. This suggests that pH may indeed be strongly dictating microbial community composition, as indicated by the fungal: bacterial dominance, when an appropriate measure of the microorganisms’ functional impact is used. 2.2.4. Soil moisture, temperature, and elevated CO2 effects Our understanding of the impact that moisture and temperature have on soil microbial communities has often been related to their role as mediators of ecosystem processes such as decomposition (Aerts, 1997). However, given the likelihood that temperature and moisture regimes are apt to change both in degree and frequency across wide geographical regions in the face of global climate change, these factors and their effect on fungal:bacterial dominance have garnered increased attention (Allison and Treseder, 2008). In general, it has been proposed that fungi will exhibit less of a response to changes in moisture than will bacteria because their chitinous cell walls make fungi more resistant and resilient to changes in moisture and temperature (Holland and Coleman, 1987). When considering the response of fungi and bacteria to changes in moisture, Frey et al. (1999) found that fungal biomass and fungal: bacterial dominance were both positively related to soil moisture in cultivated settings but bacterial biomass remained relatively constant. Studies of a related factor, the influence of dryingrewetting cycles, have resulted in disparate results; there have been suggestions that relative fungal dominance increases (Cosentino et al., 2006; Harris, 1981; Schimel et al., 1989), that relative bacterial dominance increases (Denef et al., 2001; Gordon et al., 2008) as well as little difference in fungal:bacterial dominance (Hamer et al., 2007). These diverse results may indicate system specific effects on fungi and/or bacteria. Indeed, Steenwerth et al. (2005) found that across a range of soils variation in plant communities and nutrient availability, for example, interacted with drying-rewetting treatments to affect the PLFA profiles of microbial communities. A possible explanation for this, proposed by Frey et al. (1999), is that because bacteria are generally expected to inhabit soil pore spaces whereas fungal hyphae are generally found on the exterior of soil aggregates then bacteria are physically protected from desiccation. Extending this idea, bacteria would also be less affected by mild drying/rewetting events. This is not to say that bacteria are in some way physiologically more resistant/resilient to moisture effects. It is the habitat occupied by these organisms, however, which may infer greater protection and this protection is likely related to soil texture (Six et al., 2006). Despite this theoretical rationale, a consistent pattern for drying-rewetting effects on the relative dominance of fungi:bacteria remains to be elucidated.

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The response of both bacteria and fungi to changing temperature appears to be in the same direction resulting in little to no change in fungal:bacterial dominance (Allison and Treseder, 2008; Bárcenas-Moreno et al., 2009). For example, Allison and Treseder (2008) found that the relative abundance (determined via qPCR) of both bacteria and fungi declined bye50% under experimental soil warming. This would have resulted in no change in fungal:bacterial dominance although specific fungal species were affected by warming (Allison and Treseder, 2008). Another study, found that the temperature relationships estimated with growth measurements of fungi and bacteria also responded similarly to changing temperatures (Bárcenas-Moreno et al., 2009). It appears that, in the absence of concomitant moisture effects related to temperature and barring any differences in acclimatization between these groups, there is no clear evidence that temperature itself systematically influences fungal:bacterial dominance. Elevated atmospheric CO2, in addition to any potential effects via soil moisture or temperature increases, may also impact fungal: bacterial dominance (Hu et al., 1999; Kandeler et al., 2008). However, a clear directional response of fungal:bacterial dominance to elevated CO2 has not been observed. On one hand, Lipson et al. (2005) found that under elevated CO2 fungal:bacterial dominance increased and others have noted the same (Carney et al., 2007; Kandeler et al., 2008). The potential underlying mechanism for the increase in fungal:bacterial dominance was attributed to either an increase in the recalcitrance of plant derived inputs or increased turnover of roots (Kandeler et al., 1998). On the other hand, Niklaus et al. (2003) found no increase in fungal dominance under elevated CO2 because of top-down controls imposed by fungivores and Sonnemann and Wolters (2005) noted a decrease in fungal:bacterial dominance. Denef et al. (2007) also noted no overall change in fungal:bacterial dominance but did find that AM-fungi assimilated more C under elevated CO2. It is likely that the impact elevated CO2 will have on fungal:bacterial dominance is not straightforward and will be dependent on many other factors including moisture, temperature, nutrient availability, and the interaction between these factors (Castro et al., 2010). Yet, even if there is a clear shift toward greater fungal:bacterial dominance under elevated CO2 the effect of this shift may be negligible with regards to ecosystem processes (Van Groenigen et al., 2007). 2.3. Two case studies of the functional implications of fungal: bacterial dominance Extending ideas related to the key differences between bacteria and fungi has implicated fungal:bacterial dominance as an indicator of ecosystem processes (Hendrix et al., 1986; Bardgett and McAlister, 1999; van der Heijden et al., 2008). This has led to the hypothesis that changes in fungal:bacterial dominance are likely to be related to such ecosystem processes as decomposition, nutrient cycling, C-sequestration potential, and ecosystem self-regulation (Hendrix et al., 1986; Bardgett and McAlister, 1999; Bailey et al., 2002; van der Heijden et al., 2008). As recognized by researchers in this area but still worth stressing, this relationship is susceptible to circular reasoning with fungal-dominated systems, for example, being expected to lead to greater C-sequestration rather than sites with greater C-stores simply being fungal dominant. It is the purpose of this section to explore the rationale for these linkages between fungal:bacterial dominance and ecosystem processes and to discuss the evidence for and against such linkages. Clearly, the rationale for the linkages between fungal:bacterial dominance and ecosystem processes are closely related to the environmental response of each group, as described in Section 2.2 above, and therefore some redundancy between these sections is unavoidable. We have attempted to cross reference such

occurrences. Furthermore, given the wide array of ecosystem processes that fungal:bacterial dominance may relate to we have limited ourselves to the exploration of two widely researched processes: C-sequestration and decomposition. Both should serve as sufficient case studies for the rationale which links fungal: bacterial dominance to ecosystem processes and also provide a broad overview of other ecosystem processes expected to be affected. 2.3.1. C-Sequestration and fungal:bacterial dominance An ecosystem’s C-sequestration potential has gained increased interest due to current climate change concerns (Bailey et al., 2002). The fungal:bacterial dominance of a site, given similar soil characteristics (i.e. texture, clay type, moisture), has been associated with that site’s C-sequestration potential with a greater potential associated with greater fungal:bacterial dominance (Jastrow et al., 2007). Evidence to date that relates fungal:bacterial dominance to C-sequestration has mainly been gained from comparisons of intensively managed and less intensively managed systems (also making them correlative). For example, Bailey et al. (2002) compared five land-use pairs, differing in management intensity, and found that both total soil C and fungal activity were greater for four of five pairs under less intensive management. Guggenberger et al. (1999) found the same for three of six sites but Busse et al. (2009) and Mulder and Elser (2009) found the opposite with less total soil C observed in fungal-dominated sites. Grandy et al. (2009) found that fungal:bacterial dominance was related to soil organic matter chemistry, a factor likely to impact C-sequestration, but whether changes in fungal:bacterial dominance drove or were a product of this relationship remains unclear. These ambiguous results imply that the hypothesized positive relationship between fungal dominance and C-sequestration may not be a general phenomenon. This means that an examination of those key traits expected to underlie this relationship (e.g. biomass stoichiometry, C-use efficiency, and the decomposability of their respective necromass) are necessary (Guggenberger et al., 1999; Bailey et al., 2002; Six et al., 2006; van der Heijden et al., 2008). One of these key traits is C-use efficiency (CUE) also known as growth yield efficiency (e.g. Six et al., 2006). It is expected that fungi on average produce more biomass C per unit of C metabolized than do bacteria which again leads to a greater proportion of C stored in fungal-dominated systems (high fungal:bacterial dominance) when compared to bacterial dominated systems (low fungal:bacterial dominance). Six et al. (2006) conducted an extensive review on the CUE of bacteria and fungi and found a significant degree of overlap between the two groups. More direct experimental tests conducted by Thiet et al. (2006) found no difference in CUE between sites differing in fungal:bacterial dominance. They concluded that many of the differences in CUE associated with changes in fungal:bacterial dominance were due to methodological issues. In this experiment, though, Thiet et al. (2006) only determined the amount of C mineralized and the amount remaining in the soil, and inferred fungal:bacterial dominance. They did not determine the actual accumulation of C into the biomass of the respective groups nor measure their respective biomass. Stress-events, including e.g. drying-rewetting (Section 2.2.3) and freezeethaw cycles, will lead to subsequent impacts on CUE and could affect fungi and bacteria differently. Another factor to consider is how substrate C:N influences CUE. It has been shown that as substrate C:N increases, a decrease in decomposer CUE is noted (Manzoni et al., 2008). Whether fungi in comparison to bacteria reduce their CUE less as substrate C:N increases warrants further investigation. The actual amount of time that C is stored in living fungal or bacterial biomass is another of the proposed links between fungal:


bacterial dominance and C-sequestration (Six et al., 2006). Although there are relatively few reports of biomass turnover for either group, Bååth (1994) estimated that bacterial biomass turnover ranged between days and weeks, with an average of about one week. This is comparable to values of a few days to one week reported in aquatic environments (Cole et al., 1988). A similar estimate for fungi showed that turnover was on the order of months (i.e.e130e150 days; Rousk and Bååth, 2007a) which is comparable to studies of fungal growth rates on submerged litter (e.g. Gulis et al., 2008). This suggests that C is retained longer in living fungal biomass than it is in living bacterial biomass, potentially leading to increased residence time for C associated with fungi. The decomposition of dead microbial biomass (necromass) may also potentially link fungal:bacterial dominance to C-sequestration (Guggenberger et al., 1999). This is based on the expectation that fungal necromass is more chemically recalcitrant than bacterial necromass. Fungal necromass is expected to be more chemically recalcitrant because it is composed of e.g. chitin and other potentially recalcitrant membrane components such as ergosterol (MilleLindblom et al., 2004; Zhao et al., 2005). Also, fungal biomass and in turn fungal necromass, as discussed above and in Section 2.2.2, is expected to have a wider range in C:N than bacterial biomass (McGill et al., 1981). Thus if a greater proportion of a system’s microbial necromass is composed of fungi, then the decomposition of that necromass may progress more slowly than if a greater proportion of it were derived from bacteria, that is resulting in longer residence time for C, leading to increased C-sequestration in fungal-dominated systems (Guggenberger et al., 1999). However, relatively few studies that have explicitly looked at the decomposition rates of bacterial versus fungal necromass but at least one instance found that the decomposition of fungal and bacterial necromass was equivalent (Li and Brune, 2005a). Although the necromass in this study was only sourced from one species of fungi/bacteria, it none the less demonstrates that the necromass of certain species of bacteria and fungi may be equally decomposable (Li and Brune, 2005a). On the other hand, Nakas and Klein (1979) found that the cell wall components of two bacteria species, in general, decomposed at faster rates than did three fungal species. This discrepancy may potentially be explained by the fact that Li and Brune (2005a) utilized a Gram positive bacterium whereas Nakas and Klein (1979) utilized Gram negative bacteria. Gram positive bacteria have a thick cell wall of peptidoglycan whereas Gram negative bacteria do not. Because of this difference a Gram positive’s cell wall constituents may decompose at a slower rate than a Gram negative’s or even a fungi’s. In fact, a comparison, based on two studies, of the mineralization of chitin and peptidoglycan shows that chitin has a mineralization rate equal to or w30% greater than peptidoglycan (Li and Brune, 2005a, 2005b). Differences in bacterial and fungal growth forms, with the possible exception of the actinomycetes, may lead to greater C-sequestration when a system is fungal-dominated for at least two reasons. First, if fungal hyphae grow into a habitat such as a soil aggregate or piece of wood and die, their necromass is largely protected from decomposition (Guggenberger et al., 1999; Six et al., 2006). Second, fungal activity may lead to increased aggregation via both mechanical processes (e.g. entanglement of soil particles by hyphae; Guggenberger et al., 1999; Six et al., 2006) and chemical processes (e.g. the exudation of glomalin by AM-hyphae; Guggenberger et al., 1999; Pikul et al., 2009). An increase in soil aggregation leads to incorporation of SOC into the aggregate making it biologically unavailable (Guggenberger et al., 1999; Wilson et al., 2009). As fungal dominance increases then the likelihood of either of these two occurrences may increase. Yet, many other physical and chemical properties of the soil are also likely to influence soil aggregation and fungal dominance may be only one

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of many (Wilson et al., 2009). The importance of fungal dominance as it pertains to aggregate formation and possibly C-sequestration is again an area where more research is needed. 2.3.2. Litter decomposition and fungal:bacterial dominance The decomposition of foliar leaf litter is perhaps one of the most widely studied processes in terrestrial ecosystems and is influenced by the microbial community. The role that fungi play in this process is distinct from that played by bacteria (de Boer et al., 2005; van der Wal et al., 2006; Meidute et al., 2008). As litter recalcitrance increases then the fungal role is expected to increase (van der Heijden et al., 2008). Several mechanisms have been proposed to justify this finding including stoichiometric differences and the hyphal growth form of fungi that allows them to both grow into leaf litter bypassing the more recalcitrant outer layers of the leaf, and that hyphal bridges allow fungi to alleviate nutrient limitations associated with litter decomposition by relocating limiting nutrients from other sources (Hendrix et al., 1986; Holland and Coleman, 1987). Probably the most important reason for the greater importance of fungi in the decomposition of recalcitrant litter is related to their lignin degrading ability (reviewed by de Boer et al., 2005). There is a general consensus in the literature that fungi are capable of degrading lignin whereas bacteria are not (de Boer et al., 2005; van der Heijden et al., 2008; but also see Perestelo et al., 1996; VargasGarcía et al., 2007). Additionally, fungi also dominate the decomposition of cellulose and hemi-cellulose, which are important constituents of organic matter in many systems (de Boer et al., 2005). In this section we will explore some of these mechanisms and, as above, assess the validity of relating fungal:bacterial dominance to leaf litter decomposition as well as the role both bacteria and fungi play in this process. As discussed above (see Section 2.2.2) litter C:N ratios are thought to be predictors of whether that litter is primarily decomposed by bacteria or fungi due to stoichiometric constraints. Yet, research by Güsewell and Gessner (2009) indicate that the role of fungi and bacteria in the decomposition of leaf litter may not be this clear-cut. They found that bacteria dominated the decomposition of leaf litter with a greater C:N when phosphorous (P) was not limiting and exhibited equal or greater decomposition rates compared to fungaldominated treatments. This was attributed to heterotrophic N-fixation by litter inhabiting bacteria. On the other hand fungi dominated when C:N was lower and P was limiting (Güsewell and Gessner, 2009). This could suggest that fungal growth may be stimulated by N additions, which agrees with previous reports that show increased stimulation of fungal growth when plant substrates are combined with N additions (Rousk and Bååth, 2007b). Additionally, an experimental laboratory-based study, which used antibiotics to reduce the contribution of the bacterial community to organic matter decomposition found an immediate positive response in fungal growth, which suggested competitive release (Rousk et al., 2008). The result of this switch from bacterial based to fungal based decomposition did not affect the mineralization of the plant litter. The same result was observed, using a range of different bacterial specific antibiotics, during the colonization of labile (alfalfa) and recalcitrant (straw) litter under in situ soil conditions. The functional redundancy of fungi and bacteria demonstrated in this removal experiment suggest that if fungal: bacterial dominance can affect the decomposition of plant litter short-term, the effects are very subtle. All the studies reported above are short-term (between 3 and 50 days) and may not be sufficient to evaluate the longer term effects of fungi. For example, Poll et al. (2008) found in a microcosm study that initial colonization of litter was dominated by bacteria and latter stages where dominated by fungi. This was presumably driven by bacteria mineralizing the soluble, easily-available

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compounds and leaving more recalcitrant compounds behind (Poll et al., 2008). Although this may be true in most cases, it is not true for all litter types or for all microbial communities. Strickland et al. (2009) found that in some cases bacterial dominance actually increased during decomposition and this was dependent on both the microbial community in question and the litter being decomposed. Another key argument made in favour of fungi as the dominant decomposers of recalcitrant litter resources is based on their lignin degrading abilities (Tuomela et al., 2000; de Boer et al., 2005). It has been known that fungi posses the enzymes necessary for degrading lignin but there are few documented cases of bacteria also performing this role (reviewed by de Boer et al., 2005). In fact, the shift in bacterial community composition in the presence of lignin degrading fungi is ascribed to bacteria playing a supporting and not a lead role in this process (Tornberg et al., 2003; Folman et al., 2008). However, work conducted by Vargas-García et al. (2007) questions this. They demonstrated that a greater proportion of bacterial isolates could degrade lignin than fungal isolates and that some bacteria even had a greater lignin degrading capacity than fungi. Other results have also shown similar capabilities for bacteria but whether these outcomes will hold under field settings, as demonstrated for fungi, and whether this will affect the dominance ratio between these two groups is unknown (Perestelo et al., 1996). As for C-sequestration, the most direct line of evidence in support of the greater decomposition of recalcitrant litter by fungi can be related to the fungal growth form. For instance, fungi have the ability to grow into litter material that allows them to bypass the recalcitrant outer layers of litter (Hendrix et al., 1986). This is an ability that most bacteria lack and its importance is potentially significant, but the actual benefit that this may give to fungi during decomposition remains unknown and unexplored. It also disregards the effects of other litter inhabiting organisms, such as collembola, mites, and earthworms, which may increase the surface area of litter available for bacterial colonization via fractionation (Wardle, 2002). Thus if soil fauna are in low abundance, for reasons other than a biologically unfavourable environment (e.g. saturated soils), then the role of fungi in litter decomposition may be more important but if soil fauna are in greater abundance then the role of bacteria may be as important, if not more so (Wardle, 2002). Soil fauna are also likely to have other effects on fungal:bacterial dominance during decomposition and other ecosystem processes via top-down effects (Bardgett et al., 1998; Björnlund et al., 2000; Christensen et al., 2007; Denton et al., 1999; Niklaus et al., 2003; Sonnemann and Wolters, 2005; Vestergard et al., 2004). This is an area that would greatly benefit from a more thorough assessment and synthesis. Another advantage of the fungal growth form is related to the translocation and integration of resources (including C and other nutrients) across wide spatial scales (Briones and Ineson, 1996; Frey et al., 2000, 2003). Because fungal hyphae cover great distances this allows fungi to subsidize the decomposition of a nutrient poor litter resource with nutrients translocated from a nutrient rich litter resource (Briones and Ineson, 1996; Tiunov, 2009). In fact it is this mechanism that has often been used to explain increased decomposition rates of recalcitrant litters in litter mixtures (Tiunov, 2009). This advantage of the fungal growth form though may also be negatively impacted by litter mixing and fragmentation (Butenschoen et al., 2007). Tiunov (2009) found that in litter mixtures as particle size decreases, positive effects on decomposition rates were negated. They hypothesized that inhibitory compounds, such as phenolics, could more easily diffuse throughout the litter layer thus negatively impacting microbial decomposers. It is also likely that fragmentation and mixing impact fungi in much the same way tilling does (i.e. evenly distributing nutrients; see Section 2.2.1).

3. Conclusions Fungal:bacterial dominance is a widely used metric that has provided soil ecologists the means to assess both the environmental impacts on and the functional implications of soil microbial communities. We suggest that future research in this realm should first assess the mechanism by which a change in fungal:bacterial dominance might occur. With that mechanism in mind a relevant method for determining fungal:bacterial dominance should be chosen. For example, if we want to contrast the functional contributions of the decomposer groups, we should use directly relevant growth-related measurements; If C-sequestration is the ecosystem process in question and it is decided that a build-up in the amount of fungal cell wall components are likely to influence this process then measurements of fungal residues would likely be the most applicable; and if C-sequestration is thought to be related to CUE, substrate used for growth should be compared to the amount respired. There is no one universal index that can be used to envelope all of these questions, and only the aspects of fungi and bacteria (growth, biomass, or residue, depending on context) that are directly related to the question at hand should be used. Yet, whether insights gained from such an approach are in line with current theory remains to be seen largely because our understanding of the bacteria and fungi in soil, especially regarding trait overlap, is far from complete. This highlights a fundamental basic science-imperative to more fully understand the ecology of these important organisms. Acknowledgements We gratefully thank Noah Fierer who generously inspired this entire enterprise, and hosted and moderated our initial discussions on the subject. We also thank Mark Bradford, Bobbi Helgason and Erland Bååth for useful discussion and insightful feedback on earlier drafts. We thank Steve Trudell for providing us with C:N ratios used in Fig. 2. MS was funded by the Andrew W. Mellon Foundation and JR was supported by a Swedish Research Council (VR) Postdoctoral Fellowship. Appendix. Supplementary material Supplementary data associated with this article can be found in the online version at doi:10.1016/j.soilbio.2010.05.007. References Aerts, R., 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79, 439e449. Alexander, M., 1977. Introduction to Soil Microbiology, second ed. John Wiley, New-York, 467 pp. Allison, S.D., Treseder, K.K., 2008. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology 14, 2898e2909. Anderson, J.P., Domsch, K.H., 1973. Quantification of bacterial and fungal contributions to soil respiration. Archiv Fur Mikrobiologie 93, 113e127. Arao, T., 1999. In situ detection of changes in soil bacterial and fungal activities by measuring C-13 incorporation into soil phospholipid fatty acids from C-13 acetate. Soil Biology & Biochemistry 31, 1015e1020. Aviv, M., Giladi, H., Oppenheim, A.B., Glaser, G., 1996. Analysis of the shut-off of ribosomal RNA promoters in Escherichia coli upon entering the stationary phase of growth. FEMS Microbiology Letters 140, 71e76. Bååth, E., 1992. Thymidine incorporation into macromolecules of bacteria extracted from soil by homogenization centrifugation. Soil Biology & Biochemistry 24, 1157e1165. Bååth, E., 1994. Measurement of protein-synthesis by soil bacterial assemblages with the leucine incorporation technique. Biology and Fertility of Soils 17, 147e153. Bååth, E., 1996. Adaptation of soil bacterial communities to prevailing pH in different soils. FEMS Microbiology Ecology 19, 227e237. Bååth, E., 2001. Estimation of fungal growth rates in soil using C-14-acetate incorporation into ergosterol. Soil Biology & Biochemistry 33, 2011e2018.

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Considering fungal:bacterial dominance in soils - Methods ... - CiteSeerX

Considering fungal:bacterial dominance in soils - Methods ... - CiteSeerX

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