Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem

Abstract

Biological sulfur cycling in polar, low-temperature ecosystems is an understudied phenomenon in part due to difficulty of access and the dynamic nature of glacial environments. One such environment where sulfur cycling is known to play an important role in microbial metabolisms is located at Borup Fiord Pass (BFP) in the Canadian High Arctic. Here, transient springs emerge from ice near the terminus of a glacier, creating a large area of proglacial aufeis (spring-derived ice) that is often covered in bright yellow/white sulfur, sulfate, and carbonate mineral precipitates accompanied by a strong odor of hydrogen sulfide. Metagenomic sequencing of samples from multiple sites and of various sample types across the BFP glacial system produced 31 metagenome-assembled genomes (MAGs) that were queried for sulfur, nitrogen, and carbon cycling/metabolism genes. An abundance of sulfur cycling genes was widespread across the isolated MAGs and sample metagenomes taxonomically associated with the bacterial classes Alphaproteobacteria and Gammaproteobacteria and Campylobacteria (formerly the Epsilonproteobacteria). This corroborates previous research from BFP implicating Campylobacteria as the primary class responsible for sulfur oxidation; however, data reported here suggested putative sulfur oxidation by organisms in both the alphaproteobacterial and gammaproteobacterial classes that was not predicted by previous work. These findings indicate that in low-temperature, sulfur-based environments, functional redundancy may be a key mechanism that microorganisms use to enable coexistence whenever energy is limited and/or focused by redox chemistry. IMPORTANCE A unique environment at Borup Fiord Pass is characterized by a sulfur-enriched glacial ecosystem in the low-temperature Canadian High Arctic. BFP represents one of the best terrestrial analog sites for studying icy, sulfur-rich worlds outside our own, such as Europa and Mars. The site also allows investigation of sulfur-based microbial metabolisms in cold environments here on Earth. Here, we report whole-genome sequencing data that suggest that sulfur cycling metabolisms at BFP are more widely used across bacterial taxa than predicted. From our analyses, the metabolic capability of sulfur oxidation among multiple community members appears likely due to functional redundancy present in their genomes. Functional redundancy, with respect to sulfur-oxidation at the BFP sulfur-ice environment, may indicate that this dynamic ecosystem hosts microorganisms that are able to use multiple sulfur electron donors alongside other metabolic pathways, including those for carbon and nitrogen.

Contribution Evenness: A functional redundancy metric sensitive to trait stability in microbial communities

“…The last metric is informal but has been utilized by various authors. In this approach, functional redundancy is simply interpreted as the proportion of species in a community with a trait (e.g., Trivedi, 2020; Tully, Wheat, et al, 2018; Wohl, Arora, & Gladstone, 2004).…”

“…Several metrics for functional redundancy exist in the literature. Functional redundancy has been taken as the ratio of community richness and the theoretical maximum number of functional entities (Mouillot et al, 2014), median metabolic overlap of genomic traits (Hester, Jetten, Welte, & Lücker, 2019), expected variability in trait space among community members (Ricotta et al, 2016), the degree of covariance in functional diversity and biodiversity (e.g., Galand et al, 2018; Micheli & Halpern, 2005; Miki, Yokokawa, & Matsui, 2013), and the simple fraction of a community with a given trait (Trivedi et al, 2020; Tully, Wheat, Glazer, & Huber, 2018; Wohl, Arora, & Gladstone, 2004). Notably, these different metrics treat community structure differently.…”

“…As functional redundancy is a measure of species density with respect to an ecological function, enumerating the number of “contributors” towards a community-aggregated parameter may suffice as a measure of functional redundancy. Although not explicitly stated as such, some methods we mentioned before use this approach (Trivedi et al, 2020; Tully, Wheat, et al, 2018; Wohl et al, 2004). We note that simple enumeration does not weight the variable contributions by different species, which may be desirable.…”

“…The diversity of metrics reflects the diverse sources of data used to calculate functional redundancy and the diverse purposes for how this concept has been applied. Functional redundancy has been measured as the ratio of community richness to the theoretical maximum number of functional entities (6), median metabolic overlap of genomic traits (7), expected variability in trait space among community members (8), the degree of covariance in functional diversity and biodiversity (e.g., Galand et al, 2018;Micheli & Halpern, 2005;Miki, Yokokawa, & Matsui, 2013), and the simple fraction of populations in a community that bear a given function (12)(13)(14). These different metrics treat community structure differently.…”

Divergent Genomic Adaptations in the Microbiomes of Arctic Subzero Sea-Ice and Cryopeg Brines

“…In cryopeg brines, Marinobacter contributed the most strongly to the variance from sea ice (Figure 1C), in keeping with its predominance in the cryopeg samples (46-79% of the prokaryotic community) except for CB4 (4%; Figure 2). Marinobacter representatives have been observed and isolated from a variety of other cold and saline environments, including Blood Falls, the saline subglacial outflow from Taylor Glacier, Antarctica (Mikucki and Priscu, 2007;Chua et al, 2018;Campen et al, 2019), a cold saline spring in the Canadian High Arctic (Niederberger et al, 2010;Trivedi et al, 2020), and Arctic sea ice (Zhang et al, 2008). Experimental work on isolated members (reviewed by Handley and Lloyd, 2013), as well as genomic insights into the functional capabilities of Marinobacter members (Singer et al, 2011), attribute to this genus a remarkable versatility in growth and energy acquisition strategies and a high genomic potential to adapt to challenging environmental conditions, which may have enabled Marinobacter to compete effectively for resources and reach high relative abundance (Figure 2) despite the extreme conditions in cryopeg brine.…”