Maintenance of soil functioning following erosion of microbial diversity

Abstract

The paradigm that soil microbial communities, being very diverse, have high functional redundancy levels, so that erosion of microbial diversity is less important for ecosystem functioning than erosion of plant or animal diversity, is often taken for granted. However, this has only been demonstrated for decomposition/ respiration functions, performed by a large proportion of the total microbial community, but not for specialized microbial groups. Here, we determined the impact of a decrease in soil microbial diversity on soil ecosystem processes using a removal approach, in which less abundant species were removed preferentially. This was achieved by inoculation of sterile soil microcosms with serial dilutions of a suspension obtained from the same non-sterile soil and subsequent incubation, to enable recovery of community size. The sensitivity to diversity erosion was evaluated for three microbial functional groups with known contrasting taxonomic diversities (ammonia oxidizers < denitrifiers < heterotrophs). Diversity erosion within each functional group was characterized using molecular fingerprinting techniques: ribosomal intergenic spacer analysis (RISA) for the eubacterial community, denaturing gradient gel electrophoresis (DGGE) analysis of nirK genes for denitrifiers, and DGGE analysis of 16S rRNA genes for betaproteobacterial ammonia oxidizers. In addition, we simulated the impact of the removal approach by dilution on the number of soil bacterial species remaining in the inoculum using values of abundance distribution of bacterial species reported in the literature. The reduction of the diversity of the functional groups observed from genetic fingerprints did not impair the associated functioning of these groups, i.e. carbon mineralization, denitrification and nitrification. This was remarkable, because the amplitude of diversity erosion generated by the dilution approach was huge (level of bacterial species loss was estimated to be around 99.99% for the highest dilution). Our results demonstrate that the vast diversity of the soil microbiota makes soil ecosystem functioning largely insensitive to biodiversity erosion even for functions performed by specialized groups.

Disconnect of microbial structure and function: enzyme activities and bacterial communities in nascent stream corridors

“…However, those experiments primarily focused on assessing effects of varying numbers of species or strains rather than the composition of communities and abundance of dominant strains or species as in the present study. Moreover, in line with our results, field studies that have indirectly manipulated microbial communities have not typically found evidence for strong relationships between community structure and rates of ecosystem processes (Langenheder et al, 2005Wertz et al, 2006;Ö stman et al, 2010).…”

“…These results are in line with evidence from a body of similar experiments conducted with higher plants, invertebrates, algae and other microorganisms (Gessner et al, 2010;Cardinale et al, 2011). They contrast with outcomes of indirect microbial community manipulations, for instance, by means of dilution series (Langenheder et al, 2005Wertz et al, 2006;Ö stman et al, 2010) or fumigation (Griffiths et al, 2000), which have failed to detect similar relationships. The discrepancy can be reconciled by acknowledging that key differences exist between the two approaches (Bell et al, 2009).…”

Microbial community modeling using reliability theory

“…These results are consistent with the idea that the reliability of narrowly distributed functions will be most sensitive to changes in microbial community composition (Schimel and Gulledge, 1998). In contrast, reduced diversity did not reduce the rate of the specialized functions of denitrification or ammonia oxidation in soil microcosms, where the inocula had been diluted to vary the diversity, provided the inoculum was sufficient to allow regrowth to the original abundance of the functional group (Wertz et al, 2006). Without an understanding of these fundamental relationships between community structure and function, microbial ecology is lacking a foundation, and researchers may pursue increasingly detailed molecular analyses of microbial communities without a basis for understanding when or if that information is of functional relevance.…”

Agriculture's impact on microbial diversity and associated fluxes of carbon dioxide and methane

“…Given the extensive microbial diversity in soils and the ubiquitous distribution of CO 2 -yielding metabolic pathways in heterotrophs, it is perhaps not surprising that there was no discernible relationship between diversity and soil respiration. The lack of a general relationship between bacterial diversity and soil respiration has been documented for other soil types as well (Balser and Firestone, 2005;Wertz et al, 2006). Rather than being related to bacterial diversity, we found that CO 2 production from soil was more strongly predicted by soil moisture and temperature-two well-known regulators of soil metabolism (Cook and Orchard, 2008).…”