Fungi to bacteria ratio: Historical misinterpretations and potential implications

Abstract

Bacteria and fungi are the primary consumers and, thus, the decomposition pathways are described accordingly as bacterial-based or fungal-based energy channels. However, the fungi to bacteria ratios (F: B), which indicated either by microbial biomass, respiration, or growth, represents only a snapshot of the whole energy channel during a given period rather than the cumulative contribution. Even the energy channel biomass only takes into account one dimension without considering the time. We believe that the F: B ratio has been misinterpreted in an ecological sense due to a lack of a clear definition. Here, we estimated the F: B biomass ratios, production ratios (microbial biomass multiplied by the turnover rate) and assimilation ratios (the sum of microbial production and respiration) using a dataset from 192 relevant studies. The F: B biomass ratios varied from 0.106 to 9.080, depending on the methods used. Based on direct microscopy method, the fungal/(fungal + bacterial) production and assimilation ratios ranged from 0.39 to 54.78% and 0.25–45.05%, respectively; while, those ratios based on phospholipids fatty acids (PLFAs) method were 0.06–5.51% and 0.04–0.66%, respectively. We conclude that bacteria contributes greater to the energy flow in terrestrial ecosystems compared with fungi based on the F: B assimilation. The relative contribution of bacteria and fungi can be better evaluated using the F: B assimilation ratio, rather than the biomass ratio or production ratio. Nevertheless, there are still uncertainties in the estimations of microbial production and assimilation due to their complicated responses to soil fauna activities. The regulation of soil fauna on microbial biomass, turnover rate and respiration, and associated changes in the energy allocations in the soil food web should be emphasised in future studies.

Introduction

Soil microbial communities, as principle decomposers, play critical roles in the regulation of nutrient cycling, energy flow and ecosystem productivity (Wardle, 1998; Jackson et al., 2007; Rinklebe and Langer, 2013). Soil fungi and bacteria are major microbial components with distinct physiological and ecological characteristics (van der Wal, 2006; Wang et al., 2016). For instance, bacterial biomass has a lower carbon to nitrogen (C: N) ratio (3–6), whilst fungal biomass has a higher C: N ratio (5–15) (McGill et al., 1981). Accordingly, a higher soil C: N ratio may increase the relative abundance of fungi due to stoichiometric constraints, as bacteria are generally believed to require more N per unit of biomass C accumulation than fungi (Elliott et al., 1983; Fierer et al., 2009). Therefore, the ratio of fungi to bacteria (F: B), as an indicator of microbial community structure, has important ecological significance in soil ecology (Bailey et al., 2002), and reflects the capacity of ecosystem self-regulation (Bardgett and McAlister, 1999; de Vries et al., 2006). A higher biomass ratio of fungi to bacteria is believed to indicate a more sustainable agro-ecosystem (de Vries et al., 2006). It had also been reported that a clear relationship between increasing plant productivity and bacterial versus fungal dominance (Ingham and Slaughter, 2004; de Ruiter et al., 2005).

The earliest descriptions of fungal-dominated and bacterial-dominated microbial communities appeared 40 years ago, where microbial communities in streams were reported to shift from fungal-dominated to bacterial-dominated as litter decomposition proceeded (Bärlocher and Kendrick, 1974; Suberkropp and Klug, 1976). Also, compared with fungi, a greater population of soil bacteria was observed in rotation regimes (Golebiowska and Ryszkowski, 1977). Thereafter, a large amount of researches on the effects of the different tillage systems on microorganisms has been conducted. A conventionally tilled agro-ecosystem was reported to be characterised by a bacterial-based food web; in contrast, a no-tillage system by a fungi-based food web (Hendrix et al., 1986). Meanwhile, soil food web structures amongst different ecosystems during natural succession attracted significant attention. It was found to change gradually from the bacterial-based grassland ecosystem to the fungal-based forest ecosystem (Ingham et al., 1986a, 1986b; 1989; Ingham and Thies, 1996). A large number of plants with high-quality (high nitrogen and low tannin) litter is beneficial to the growth of bacteria in the early succession, but in late stage of succession, plants with low-quality (low nitrogen and high tannin) litter generate and then promote the growth of fungi (Ohtonen et al., 1999). Note that these previous studies were based on the dilution plate or direct microscopy counting method, and the reported F: B ratios were normally >1.0 which may overemphasize the contribution of fungi.

F: B ratios were then extensively studied with the gradual development of methodology for microbial studies, such as phospholipid fatty acids (PLFAs), substrate-induced respiration (SIR) and 16S or 18S DNA sequencing (Frostegård and Bååth, 1996; Bailey et al., 2002; Fierer et al., 2009). In addition, the concept of bacterial channel or fungal channel was introduced to consider the biomasses of both bacteria and fungi and their feeders (Ruess and Ferris, 2004). Strong associations between nematodes and their fungal or bacterial food sources were revealed. The bacterial-dominated soils have many bacterial predators (e.g., protozoa and bacterial-feeding nematodes), whilst fungal-dominated soils have many fungal predators (e.g., fungal-feeding nematodes and fungal-feeding microarthropods) (Ingham et al., 1989). Subsequently, Ruess and Ferris (2004) proposed that consumer organisms affect the rates of energy and nutrient release. The nature and abundance of available resources can be monitored by faunal analysis of fungal- and bacterial-feeding nematodes. Pathways with a strong bacterial component generally occur in N-rich soils that contain readily decomposable substrates. Zhao and Neher (2014) analysed 67 raw data sets of nematode genera from the three types of ecosystems and concluded that energy pathways are bacterial-dominated in all ecosystems whether expressed as nematode abundance or biomass. Furthermore, both bacteria and fungi support their soil fauna predator in the corresponding food chain (de Ruiter et al., 1993; Wardle and Lavelle, 1997). Hence, it was proposed that bacterial channel biomass is the sum of bacteria and bacterial-feeding fauna, and fungal channel biomass is the sum of fungi and fungal-feeding fauna (Holtkamp et al., 2008; de Vries et al., 2012b).

In the abovementioned studies, the F: B biomass ratios were sometimes greater than 1.0 (Ingham et al., 1989; Ohtonen et al., 1999). Also, the F: B channel biomass ratios were sometimes greater than 1.0, indicating there are fungal-based ecosystems in grassland (de Vries et al., 2012b, 2012c). However, it may not be appropriate to determine the relative fungal or bacterial dominance only by the F: B standing biomass ratio. Soil microbial biomass is controlled by two distinct processes: changes in biomass production in biomass destruction (e.g., predation, physical disruption or microbial death); thus, the standing biomass is only a snapshot of the outcome of these processes. In contrast, the microbial metabolic quotient (respiration: biomass ratio) can reflect the ecological efficiency of fungi and bacteria (Beare et al., 1992; Blagodatskaya and Anderson, 1998). As a result, the microbial biomass markers may be largely unrelated to their contributions to processes such as carbon mineralisation and nutrient cycling (Bapiri et al., 2010). In other words, standing microbial biomass may account for much less proportions of the total energy flow due to the ignorance of microbial turnover and respiration.

Overall, a wide variety of conceptual terms regarding the F: B ratios have gradually emerged, and we believe that the F: B ratio has been misinterpreted in an ecological sense due to a lack of a clear definition. For a better understanding of the F: B ratios, we summarised and explain the various terms of F: B ratios, e.g., F: B biomass ratio, F: B activity or respiration ratio, F: B gene ratio, F: B growth ratio and F: B channel biomass ratio (Table 1). Given that assimilation may reflect the contribution of fungi or bacteria to the energy flow in ecosystems (Odum, 1957), we used F: B production, as well as F: B assimilation ratios, to quantify the relative dominance of fungi or bacteria. We collected data on the F: B ratios in terms of biomass, production and assimilation from literature as well as from our own experiments, and summarised the patterns of F: B ratios in different ecosystems. The specific steps are as follows: 1) collecting the F: B ratios in term of biomass from literature; 2) collecting the turnover time of bacteria and fungi in different ecosystem, then the F: B biomass was multiplied by the turnover time to obtain the F: B production ratio per unit of time (Carter and Suberkropp, 2004; Appendix S3). 3) collecting the ratio of production to respiration for bacteria and fungi (Holland and Coleman, 1987), then calculating the assimilation of bacteria or fungi per unit of time equaled the sum of the production and the respiration of bacteria or fungi at a trophic level (Odum, 1957). Our objectives were to 1) demonstrate the effect of microbial turnover, production and respiration on the F: B ratios in different ecosystems; 2) compare various expressions of F: B ratios and differences of their interpretations; and 3) estimate the relative contribution of fungi and bacteria to energy flow at a trophic level.