Glacier shrinkage will accelerate downstream decomposition of organic matter and alters microbiome structure and function

Abstract

The shrinking of glaciers is among the most iconic consequences of climate change. Despite this, the downstream consequences for ecosystem processes and related microbiome structure and function remain poorly understood. Here, using a space-for-time substitution approach across 101 glacier-fed streams (GFSs) from six major regions worldwide, we investigated how glacier shrinkage is likely to impact the organic matter (OM) decomposition rates of benthic biofilms. To do this, we measured the activities of five common extracellular enzymes and estimated decomposition rates by using enzyme allocation equations based on stoichiometry. We found decomposition rates to average 0.0129 (% d^-1 ), and that decreases in glacier influence (estimated by percent glacier catchment coverage, turbidity, and a glacier index) accelerates decomposition rates. To explore mechanisms behind these relationships, we further compared decomposition rates with biofilm and stream water characteristics. We found that chlorophyll-a, temperature, and stream water N:P together explained 61% of the variability in decomposition. Algal biomass, which is also increasing with glacier shrinkage, showed a particularly strong relationship with decomposition, likely indicating their importance in contributing labile organic compounds to these carbon-poor habitats. We also found high relative abundances of chytrid fungi in GFS sediments, which putatively parasitize these algae, promoting decomposition through a fungal shunt. Exploring the biofilm microbiome, we then sought to identify bacterial phylogenetic clades significantly associated with decomposition, and found numerous positively (e.g., Saprospiraceae) and negatively (e.g., Nitrospira) related clades. Lastly, using metagenomics, we found evidence of different bacterial classes possessing different proportions of EEA-encoding genes, potentially informing some of the microbial associations with decomposition rates. Our results, therefore, present new mechanistic insights into OM decomposition in GFSs by demonstrating that an algal-based "green food web" is likely to increase in importance in the future and will promote important biogeochemical shifts in these streams as glaciers vanish.

Keywords: alpine biogeochemistry; carbon cycling; ecological stoichiometry; extracellular enzyme activity; microbial ecology.

FIGURE 1

Decomposition rates exhibited a wide range of values across glacier‐fed streams, and were significantly greater at downstream (DN) versus upstream (UP) transects. We collected stream sediments from 101 glacier‐fed streams (GFSs) from six major global regions, including the European Alps (green, n = 27 GFSs), Russian Caucasus (orange, n = 19 GFSs), Ecuadorian Andes (blue, n = 15 GFSs), Greenland (violet, n = 10 GFSs), Norway (green, n = 10 GFSs), and New Zealand (yellow, n = 20 GFSs). At each GFS, two transects were sampled (up‐ and downstream), and at each transect three patches for a total of 606 individual measurements for decomposition rate, here expressed as natural log‐transformed % day⁻¹

FIGURE 2

Decomposition rate increases with decreasing glacier influence using a space for time substitution. Decomposition rates in glacier‐fed streams were negatively associated with the (a) glacier index, (b) percent glacier coverage of catchments, and (c) stream water turbidity (all natural log‐transformed), suggesting that decomposition rates will increase with glacier shrinkage. Generalized additive models for location, scale and shape (GAMLSS) identified a significant decrease in the mean (black line), but an increase in variance (dashed gray line) in modeled decomposition rates with increases in all three variables (glacier index: μ, df = 3; t‐value = −21.47; p < 0.001; σ, df = 3; t‐value = 8.19; p < 0.001; percent glacier coverage: μ, df = 3; t‐value = −11.75; p < 0.001; σ, df = 3; t‐value = 5.88; p < 0.001; stream water turbidity: μ, df = 3; t‐value = −20.36; p < 0.001; σ, df = 3; t‐value = 6.06; p < 0.001)

FIGURE 3

Decomposition in glacier‐fed streams is related to organic matter availability and subject to temperature and stoichiometric constraints. Chlorophyll a (a), stream water temperature (b), and stream water molar N:P ratios (c) all have significant positive univariate associations with modeled decomposition rates (all natural log‐transformed). For all three, GAMLSS identified a significant increase in the mean (black line), but an decrease in variance (dashed grey line) in modeled decomposition rates with increases in all three variables (chlorophyll a; μ, df = 3; t‐value = 26.61; p < .001; σ, df = 3; t‐value = −8.54; p < .001; temperature; μ, df = 3; t‐value = 5.93; p < .001; σ, df = 3; t‐value = −2.52; p < .001; stream water N:P; μ, df = 3; t‐value = 5.61; p < .001; σ, df = 3; t‐value = −3.56; p < .001)

FIGURE 4

Multiple bacterial clades covary with decomposition rates in the sediment biofilm microbiome across 101 glacier‐fed streams. Phylogenetic tree showing significant positively (green) and negatively (red) associated phylogenetic clades with decomposition after controlling for the effect of the sampled region. Consensus taxonomies are shown next to each clade. For the large green clade on the right the outgroup was the adjacent large red clade. For all other clades, the outgroup was the rest of the phylogeny

FIGURE 5

Bacterial classes differed in the number of gene copies for measured extracellular enzymatic activity that could be mapped through shotgun metagenomics. Relative abundance of the gene copies of a given enzyme mapped to bacterial classes are plotted against the relative abundance of a given bacterial class from 16S rRNA gene amplicon sequencing. A 1:1 line is provided for comparison. Extracellular enzymes include α‐1,4‐glucosidase, β‐1,4‐glucosidase, leucine aminopeptidase, β‐1,4‐N‐acetylglucosaminidase, and acid (alkaline) phosphatase