The microbiome of alpine snow algae shows a specific inter-kingdom connectivity and algae-bacteria interactions with supportive capacities

Abstract

Mutualistic interactions within microbial assemblages provide a survival strategy under extreme conditions; however, little is known about the complexity of interaction networks in multipartite, free-living communities. In the present study, the interplay within algae-dominated microbial communities exposed to harsh environmental influences in the Austrian Alps was assessed in order to reveal the interconnectivity of eukaryotic and prokaryotic inhabitants. All analyzed snowfields harbored distinct microbial communities. Network analyses revealed that mutual exclusion prevailed among microalgae in the alpine environment, while bacteria were mainly positively embedded in the interaction networks. Especially members of Proteobacteria , with a high prevalence of Oxalobacteraceae , Pseudomonadaceae , and Sphingomonadaceae showed genus-specific co-occurrences with distinct microalgae. Co-cultivation experiments with algal and bacterial isolates confirmed beneficial interactions that were predicted based on the bioinformatic analyses; they resulted in up to 2.6-fold more biomass for the industrially relevant microalga Chlorella vulgaris , and up to 4.6-fold increase in biomass for the cryophilic Chloromonas typhlos . Our findings support the initial hypothesis that microbial communities exposed to adverse environmental conditions in alpine systems harbor inter-kingdom supportive capacities. The insights into mutualistic inter-kingdom interactions and the ecology of microalgae within complex microbial communities provide explanations for the prevalence and resilience of such assemblages in alpine environments.

Alpine Snow Algae Microbiome Diversity in the Coast Range of British Columbia

“…Across all samples, we found 173 algal, 2,739 bacterial, 380 fungal, and 540 protist/animalia operational taxonomic units (OTUs). We did not find any significant co-occurrence patterns, even when examining the specific genera highlighted by Krug et al (2020). We found only seven bacterial, one fungal, and two glissomonad OTUs that were present in more than 90% of snow algae samples.…”

“…As Sphingobacteriaceae are a prolific group in terms of abundance and distribution, they likely play an important role in biogeochemical cycling within the snow algae microbiome. Genomic analysis of these A B C FIGURE 5 | Correlation matrices of the taxa reported by Krug et al (2020) to be correlated with snow algal taxa in the Alps. All correlations were calculated using Kendall's tau rank correlations ( ).…”

“…Previously, we reported that Sanguina and Chloromonas dominated distinct blooms and that they were found at different elevations (Engstrom et al, 2020). Based on the work of Terashima et al (2017) and Krug et al (2020), we predicted that specific microbial taxa would be associated with the distinct algal blooms.…”

“…Because the algal communities were different (three of the blooms were red and one was green), the authors suggest that different algal species might recruit different bacterial assemblages. Another alpine study, this one in the Austrian Alps by Krug et al (2020), reports that specific algal genera from red (n = 3), green (n = 1), and orange (n = 1) patches of snow positively correlate with specific bacterial genera.…”

Distribution and biogeography of Sanguina snow algae: Fine‐scale sequence analyses reveal previously unknown population structure

“…Most snow algal taxa belong to the Chlamydomonadales (Chlorophyta) but they can also be found within the Euglenophyta, Cryptophyta, and Chrysophyta among others, albeit with scant representation (Hoham & Remias, 2020). Snow phycological systems have historically been underexplored, with relatively few active researchers (Hoham, 1980; Hoham & Duval, 2001; Kol, 1968; Weiss, 1983), but recently there has been a renaissance of sorts where global investigations into these algae and associated communities have grown extensively (Anesio, Lutz, Chrismas, & Benning, 2017; Brown & Jumpponen, 2019; Brown, Olson, & Jumpponen, 2015; Brown, Ungerer, & Jumpponen, 2016; Davey et al., 2019; Hamilton & Havig, 2017, 2020; Krug, Erlacher, Markut, Berg, & Cernava, 2020; Lutz et al., 2016; Lutz, McCutcheon, McQuaid, & Benning, 2018; Lutz, Prochazkova, Benning, Nedbalova, & Remias, 2019; Müller, Bleiss, Martin, Rogaschewski, & Fuhr, 1998; Procházková, Leya, Křížková, & Nedbalová, 2019; Procházková, Remias, Řezanka, & Nedbalová, 2018; Remias, Procházková, Holzinger, & Nedbalová, 2018; Remias, Procházková, Nedbalová, Andersen, & Valentin, 2020; Segawa et al., 2018; Takeuchi, 2013; Yoshimura, Kohshima, & Ohtani, 1997). While snow algae are diverse, perhaps the most well known are algae that form red blooms in late season open field snows caused by the recently established genus Sanguina (Procházková et al, 2019) [previously assigned to Chlamydomonas cf.…”