Trophic and symbiotic links between obligate-glacier water bears (Tardigrada) and cryoconite microorganisms

Abstract

Insights into biodiversity and trophic webs are important for understanding ecosystem functions. Although the surfaces of glaciers are one of the most productive and biologically diverse parts of the cryosphere, the links between top consumers, their diet and microbial communities are poorly understood. In this study, for the first time we investigated the relationships between bacteria, fungi and other microeukaryotes as they relate to tardigrades, microscopic metazoans that are top consumers in cryoconite, a biologically rich and productive biogenic sediment found on glacier surfaces. Using metabarcoding (16S rDNA for bacteria, ITS1 for fungi, and 18S rDNA for other microeukaryotes), we analyzed the microbial community structures of cryoconite and compared them with the community found in both fully fed and starved tardigrades. The community structure of each microbial group (bacteria, fungi, microeukaryotes) were similar within each host group (cryoconite, fully fed tardigrades and starved tardigrades), and differed significantly between groups, as indicated by redundancy analyses. The relative number of operational taxonomic units (ZOTUs, OTUs) and the Shannon index differed significantly between cryoconite and tardigrades. Species indicator analysis highlighted a group of microbial taxa typical of both fully fed and starved tardigrades (potential commensals), like the bacteria of the genera Staphylococcus and Stenotrophomonas, as well as a group of taxa typical of both cryoconite and fully fed tardigrades (likely part of the tardigrade diet; bacteria Flavobacterium sp., fungi Preussia sp., algae Trebouxiophyceae sp.). Tardigrades are consumers of bacteria, fungi and other microeukaryotes in cryoconite and, being hosts for diverse microbes, their presence can enrich the microbiome of glaciers.

Tardigrade Community Microbiomes in North American Orchards Include Putative Endosymbionts and Plant Pathogens

“…This study examined the microbiota of the full tardigrade community from a particular substrate sample, in contrast to previous surveys that studied isolated species, often from laboratory cultures ( Vecchi et al, 2018 ; Kaczmarek et al, 2020 ; Mioduchowska et al, 2021 ; Zawierucha et al, 2022 ). While the focus of the current study was the bacteria associated with the full tardigrade community in a given sample, it is of course also desirable to identify species-specific tardigrade microbiota, as Vecchi et al (2018) found that tardigrade-associated bacteria varied among tardigrade species, and we encourage further research on bacteria associated with individual tardigrade species.…”

“…All tardigrade microbiome surveys, including the current study, employed laboratory technique to reduce contamination by washing the tardigrades in sterile water before DNA extraction ( Vecchi et al, 2018 ; Kaczmarek et al, 2020 ; Mioduchowska et al, 2021 ; Zawierucha et al, 2022 ). Working in a sterile environment further decreases contamination; therefore, Zawierucha et al (2022) extracted tardigrades from substrate in a sterile environment (laminar flow chamber), and we worked in a sterile field created by a Bunsen burner throughout the experiment.…”

“…All tardigrade microbiome surveys, including the current study, employed laboratory technique to reduce contamination by washing the tardigrades in sterile water before DNA extraction ( Vecchi et al, 2018 ; Kaczmarek et al, 2020 ; Mioduchowska et al, 2021 ; Zawierucha et al, 2022 ). Working in a sterile environment further decreases contamination; therefore, Zawierucha et al (2022) extracted tardigrades from substrate in a sterile environment (laminar flow chamber), and we worked in a sterile field created by a Bunsen burner throughout the experiment. Three previous studies included one type each of negative controls recommended by the RIDE standards for low biomass studies ( Eisenhofer et al, 2019 ; DNA extraction blank in ( Mioduchowska et al, 2021 ), sampling blank in ( Kaczmarek et al, 2020 ), and no-template amplification control in ( Zawierucha et al, 2022 )).…”

“…Most recently, Zawierucha et al sequenced 16S rRNA, ITS1, and 18S rRNA genes to identify bacteria, fungi, and microeukaryotes, respectively, associated with the glacial tardigrade Cryobiotus klebelsbergi (Mihelčič, 1959; Zawierucha et al, 2022 ). Cryobiotus klebelsbergi were collected from cryoconite on the surface of Forni Glacier in Italy; DNA was extracted from four samples immediately and from another three after starving for 3 weeks.…”

“…and Ferruginibacter sp. were the second most abundant bacteria in fed and starved tardigrades, respectively ( Zawierucha et al, 2022 ).…”