Heterotrophic microbial communities use ancient carbon following glacial retreat

Abstract

When glaciers retreat they expose barren substrates that become colonized by organisms, beginning the process of primary succession. Recent studies reveal that heterotrophic microbial communities occur in newly exposed glacial substrates before autotrophic succession begins. This raises questions about how heterotrophic microbial communities function in the absence of carbon inputs from autotrophs. We measured patterns of soil organic matter development and changes in microbial community composition and carbon use along a 150-year chronosequence of a retreating glacier in the Austrian Alps. We found that soil microbial communities of recently deglaciated terrain differed markedly from those of later successional stages, being of lower biomass and higher abundance of bacteria relative to fungi. Moreover, we found that these initial microbial communities used ancient and recalcitrant carbon as an energy source, along with modern carbon. Only after more than 50 years of organic matter accumulation did the soil microbial community change to one supported primarily by modern carbon, most likely from recent plant production. Our findings suggest the existence of an initial stage of heterotrophic microbial community development that precedes autotrophic community assembly and is sustained, in part, by ancient carbon.

Figure 1

Isotopic patterns in organic carbon with terrain age and potential carbon inputs. Data shown are as follows: (a) radiocarbon content (¹⁴C in % modern) of soil and (c) potential carbon inputs, including organic material under the glacier (SUG), on the glacier surface (cryoconite; SOG) and organic carbon from soils of lateral slopes (LAT); (b) stable (¹³C) carbon isotope ratios of soil and (d) potential carbon inputs; (e) radiocarbon and (f) stable isotope composition of soil respired CO₂. (a,b) Filled circles, bulk soil; triangles, humic acid fraction; open squares, humin fraction. All ¹³C data are means±1 s.d. (n=6), expressed relative to the international Vienna Pee Dee Belemnite (V-PDB). For ¹⁴C analysis, the six replicates were pooled and analysed as a composite sample.

Figure 2

Patterns of microbial community composition with terrain age. (a) Microbial community composition analysed by principal components analysis (PCA). Data are PCA axis 1 for each site (mean±1 s.d.). PCA1 explains 95.3% of the variation in microbial community composition and differs significantly with terrain age (ANOVA, F_5,29=25.2, p<0.0001). PCA1 was positively correlated with an increase in all individual PLFAs (r=0.838–0.996) and hence represents an increase in total PLFA. (b) Total PLFA (nmol g⁻¹ dry soil) and (c) fungal-to-bacterial PLFA ratio.