Picky, hungry eaters in the cold: persistent substrate selectivity among polar pelagic microbial communities.

Andrew D Steen,Carol Arnosti

doi:10.3389/fmicb.2014.00527

Abstract

Polar pelagic microbial communities access a narrower range of polysaccharide substrates than communities at lower latitudes. For example, the glucose-containing polysaccharide pullulan is typically not hydrolyzed in fjord waters of Svalbard, even though pullulan is rapidly hydrolyzed in sediments from Svalbard fjords, other polysaccharides are hydrolyzed rapidly in Svalbard waters, and pullulan is hydrolyzed rapidly in temperate waters. The purpose of this study was to investigate potential factors preventing hydrolysis of pullulan in Svalbard fjord waters. To this end, in two separate years, water from Isfjorden, Svalbard, was amended with different carbon sources and/or additional nutrients in order to determine whether increasing the concentration of these potentially-limiting factors would lead to measurable enzymatic activity. Addition of nitrate, phosphate, glucose, or amino acids did not yield detectable pullulan hydrolysis. The only treatment that led to detectable pullulan hydrolysis was extended incubation after the addition of maltotriose (a subunit of pullulan, and potential inducer of pullulanase). In these fjords, the ability to enzymatically access pullulan is likely confined to numerically minor members of the pelagic microbial community. These results are consistent with the hypothesis that pelagic microbial communities at high latitudes exhibit streamlined functionality, focused on a narrower range of substrates, than their temperate counterparts.

Highlights

Surface ocean microbial communities differ systematically in their abilities to enzymatically hydrolyze high molecular weight organic matter, and to initiate remineralization of high molecular weight substrates (Arnosti et al, 2011)
The observation that addition of maltotriose led to measurable pullulanase activity after sufficient pre-incubation is consistent with biochemical control of pullulanase expression, since pullulan is composed of repeating units of maltotriose
Oligomers of the polysaccharide induce further expression of the hydrolase, while monomers of the polysaccharide repress expression of the homologous hydrolase. This regulation mechanism has been demonstrated for thermophilic bacteria that hydrolyze pullulan (Antranikian, 1990); the current data suggest that pullulanase activity in Svalbard waters may be regulated in a similar manner

Summary

Introduction

Surface ocean microbial communities differ systematically in their abilities to enzymatically hydrolyze high molecular weight organic matter, and to initiate remineralization of high molecular weight substrates (Arnosti et al, 2011). Pelagic microbial communities at high latitude are capable of hydrolyzing a narrower spectrum of soluble substrates than their temperate counterparts, the underlying reasons for this substrate selectivity are unknown. Substrate consumption in Arctic microbial communities is affected by a wide range of factors, including season, location, and nutrient levels (Kirchman et al, 2009b; Nikrad et al, 2012). The functional difference in enzyme activities observed over latitudinal gradients, and the narrow spectrum of substrates hydrolyzed by Arctic microbial communities, may be driven by a lack of a nutrient or co-factor required to induce production of specific enzymes by organisms possessing them, or by a lack of organisms with the genes to synthesize the enzymes required to hydrolyze specific substrates

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