Resolving Drivers of Microbial Community Structure in The Dry Valleys of Antarctica

Understanding the processes that underlie patterns of microbial distribution is fundamental to the field of microbial ecology, but extremely challenging given the complexity of natural systems. Antarctica’s ice-free regions possess unique ecosystems of simple trophic structure, shaped by the harsh environmental conditions that typify the continent. The Dry Valleys comprise the largest of these regions and have one of the simplest food webs on the planet, making them a tractable system to comprehensively define relationships that influence microbial distributions at the landscape scale. The New Zealand Terrestrial Antarctic Biocomplexity Survey (nzTABS) was aimed at identifying factors that control, and can predict, biological distributions in the Dry Valleys. As part of nzTABS, the goal of the research presented in this thesis was to elucidate the factors that influence bacterial community structure in Dry Valley soils. This study explored how topographic, physicochemical, and spatial variation influence bacterial diversity and community structure across a Dry Valley landscape. Bacterial communities were characterized in 471 soil samples using automated ribosomal intergenic spacer analysis (ARISA). Diversity and community composition were most strongly related to variation in physicochemical soil properties, though significant relationships with topographic and spatial variables were also observed. This identified, for the first time, the influence of environmental variables on bacterial diversity and community composition across the landscape, and presents a structural equation model identifying those relationships. The phylogenetic diversity of bacterial communities in Dry Valley soils was also examined. High-throughput sequencing of 16S rRNA gene amplicons was used to analyze bacterial communities in 177 soil samples. This work identified significant relationships between the relative abundances of bacterial taxa and both abiotic and biotic variables, though these relationships explained only a small amount of community variation collectively. The relative abundances of several bacterial taxa were, however, significantly coupled to one another, suggesting that interactions between bacterial taxa may influence community compositions. Lastly, the bacterial composition of aerosols above the Dry Valleys was examined. High-throughput sequencing of 16S rRNA gene amplicons was used to analyze two aerosol samples collected in the Miers Valley, and their compositions were compared to those of previously characterized aerosols and soils from across the continent. Bacteria present in the aerosols were found to be distinct from those of local soils; instead, aerosol compositions were more similar to those of air samples reported from elsewhere on the planet. Importantly, these findings suggest that local redistribution of Dry Valley soil bacteria through atmospheric processes may be largely restricted to periods when high winds mobilize soil particles and associated biota. This study provides novel insights into the microbial ecology of the Dry Valleys. Despite the relative simplicity of the ecosystem, the factors that influence bacterial distributions within the Dry Valleys appear to be highly complex, and include a combination of abiotic and biotic drivers. Continued research will help to disentangle relationships that influence microbial community compositions in Antarctica’s ice-free ecosystems, and will improve understanding of processes that influence microbial community assembly globally

Airborne bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica

Bacteria are assumed to disperse widely via aerosolized transport due to their small size and resilience. The question of microbial endemicity in isolated populations is directly related to the level of airborne exogenous inputs, yet this has proven hard to identify. The ice-free terrestrial ecosystem of Antarctica, a geographically and climatically isolated continent, was used to interrogate microbial bio-aerosols in relation to the surrounding ecology and climate. High-throughput sequencing of bacterial ribosomal RNA (rRNA) genes was combined with analyses of climate patterns during an austral summer. In general terms, the aerosols were dominated by Firmicutes, whereas surrounding soils supported Actinobacteria-dominated communities. The most abundant taxa were also common to aerosols from other continents, suggesting that a distinct bio-aerosol community is widely dispersed. No evidence for significant marine input to bio-aerosols was found at this maritime valley site, instead local influence was largely from nearby volcanic sources. Back trajectory analysis revealed transport of incoming regional air masses across the Antarctic Plateau, and this is envisaged as a strong selective force. It is postulated that local soil microbial dispersal occurs largely via stochastic mobilization of mineral soil particulates

Rapid microbial dynamics in response to an induced wetting event in Antarctic Dry Valley Soils

The cold deserts of the McMurdo Dry Valleys (MDV), Antarctica, host a high level of microbial diversity. Microbial composition and biomass in arid vs. ephemerally wetted regions are distinctly different, with wetted communities representing hot spots of microbial activity that are important zones for biogeochemical cycling. While climatic change is likely to cause wetting in areas not historically subject to wetting events, the responses of microorganisms inhabiting arid soils to water addition is unknown. The purpose of this study was to observe how an associated, yet non-wetted microbial community responds to an extended addition of water. Water from a stream was diverted to an adjacent area of arid soil with changes in microbial composition and activities monitored via molecular and biochemical methods over 7 weeks. The frequency of genetic signatures related to both prokaryotic and eukaryotic organisms adapted to MDV aquatic conditions increased during the limited 7 week period, indicating that the soil community was transitioning into a typical “high-productivity” MDV community. This work is consistent with current predictions that MDV microbial communities in arid regions are highly sensitive to climate change, and further supports the notion that changes in community structure and associated biogeochemical cycling may occur much more rapidly than predicted

Nematodes in a polar desert reveal the relative role of biotic interactions in the coexistence of soil animals.

Abiotic factors are major determinants of soil animal distributions and their dominant role is pronounced in extreme ecosystems, with biotic interactions seemingly playing a minor role. We modelled co-occurrence and distribution of the three nematode species that dominate the soil food web of the McMurdo Dry Valleys (Antarctica). Abiotic factors, other biotic groups, and autocorrelation all contributed to structuring nematode species distributions. However, after removing their effects, we found that the presence of the most abundant nematode species greatly, and negatively, affected the probability of detecting one of the other two species. We observed similar patterns in relative abundances for two out of three pairs of species. Harsh abiotic conditions alone are insufficient to explain contemporary nematode distributions whereas the role of negative biotic interactions has been largely underestimated in soil. The future challenge is to understand how the effects of global change on biotic interactions will alter species coexistence

A communal catalogue reveals Earth's multiscale microbial diversity

Our growing awareness of the microbial world's importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth's microbial diversity.Peer reviewe

A communal catalogue reveals Earth’s multiscale microbial diversity

Our growing awareness of the microbial world’s importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth’s microbial diversity

Biodiversity and activity of microbial mat communities from Canadian high Arctic ice shelf ecosystems

Microbial mats exist in freshwater pools atop the Ward Hunt and Markham ice shelves in the Canadian high Arctic. In this study, culture-dependent and culture-independent techniques were used to describe the microbial diversity and activity of these mat communities.Bacterial and archaeal 16S rRNA gene clone libraries were constructed from Markham and Ward Hunt mat samples. Bacterial libraries from both mats had high diversity, though the Markham library appeared more diverse than the Ward Hunt library. Over 95% of sequences in both bacterial libraries, and all isolates from both mats, grouped within the phyla Bacteroidetes, Proteobacteria, and Actinobacteria. Archaeal diversity appeared low in both mats. Only one phylotype, potentially representing a novel Euryarchaeota, was observed in both archaeal libraries. Populations in both communities showed activity at subzero temperatures, with growth of isolates at -5°C and detectable metabolic activity at -10°C, measured by radiorespiration assays of mat microcosms

Prokaryotic diversity of arctic ice shelf microbial mats

The prokaryotic diversity and respiratory activity of microbial mat communities on the Markham Ice Shelf and Ward Hunt Ice Shelf in the Canadian high Arctic were analysed. All heterotrophic isolates and > 95% of bacterial 16S rRNA gene clone library sequences from both ice shelves grouped within the phyla Bacteroidetes, Proteobacteria and Actinobacteria. Clone library analyses showed that the bacterial communities were diverse and varied significantly between the two ice shelves, with the Markham library having a higher estimated diversity (Chao1 = 243; 105 operational taxonomic units observed in 189 clones) than the Ward Hunt library (Chao1 = 106; 52 operational taxonomic units observed in 128 clones). Archaeal 16S rRNA gene clone libraries from both ice shelves were dominated by a single Euryarchaeota sequence, which appears to represent a novel phylotype. Analyses of community activity by radiorespiration assays detected metabolism in mat samples from both ice shelves at temperatures as low as -10\ub0C. These findings provide the first insight into the prokaryotic biodiversity of Arctic ice shelf communities and underscore the importance of these cryo-ecosystems as a rich source of microbiota that are adapted to extreme cold.NRC publication: Ye

Islands in the sand : are all hypolithic microbial communities the same?

Hypolithic microbial communities (hypolithons) are complex assemblages of phototrophic and heterotrophic organisms associated with the ventral surfaces of translucent minerals embedded in soil surfaces. Past studies on the assembly, structure and function of hypolithic communities have tended to use composite samples (i.e. bulked hypolithic biomass) with the underlying assumption that samples collected from within a ‘homogeneous’ locality are phylogenetically homogeneous. In this study, we question this assumption by analysing the prokaryote phylogenetic diversity of multiple individual hypolithons: i.e. asking the seemingly simple question of ‘Are all hypolithons the same’? Using 16S rRNA gene-based phylogenetic analysis of hypolithons recovered for a localized moraine region in the Taylor Valley, McMurdo Dry Valleys, Antarctica, we demonstrate that these communities are heterogeneous at very small spatial scales (<5 m). Using null models of phylogenetic turnover, we showed that this heterogeneity between hypolithons is probably due to stochastic effects such as dispersal limitations, which is entirely consistent with the physically isolated nature of the hypolithic communities (‘islands in the sand’) and the almost complete absence of a liquid continuum as a mode of microbial transport between communities.SUPPLEMENTARY FIGURES : FIGURE S1. Moraine pavement sampling location at New Harbour, Lower Taylor Valley, East Antarctica. FIGURE S2. Barplot of mean relative abundance of the 10 most abundant genera the hypolith communities. FIGURE S3. Distribution of genera as a function of number of samples in which they are present. Red dots represent taxa that are present in more than 90% of samples and are therefore considered “generalist” taxa. FIGURE S4. Significant differences in relative abundances of phyla across hypolith communities. Community clusters are colored according to the color-coding used throughout this study: Red- Group A; Green – Group B; Blue – Group C; Purple – Group D. FIGURE S5. Decay of shared taxa between two or more samples as a function of physical distance (in metres). Points represent pair-wise comparisons between. Number of shared taxa is expressed as the zeta score. The trend line of the regression of points according to distance is represented by the solid red line, while the 95% confidence interval is represented by the dashed red lines. The trend line shows no significant decay in the number of shared taxa as distance increases between samples. FIGURE S6. Distribution of β-NTIs across all pair-wise comparisons between hypolith communities, expressed as percentage of total comparisons. Values expected if only stochastic processes drive phylogenetic turnover of communities are represented within the red trace lines (β-NTInull).TABLE S1. GPS coordinated of the hypolith samples used in this study.TABLE S2. Main topological features of the taxa used to generate the interaction network, together with their functional predictions according to the FAPROTAX database.TABLE S3. RCbray values for pairwise comparisons with | β-NTI| <2, together with the significance of the results. The groups to which each sample in the comparison belong to are shown in the ‘Groups’ column, with letters in bold representing comparisons within the same group.DATA AVAILABITY : The raw sequencing reads can be found in the NCBI Bioproject database (BioProject ID:PRJNA659625, https://www.ncbi.nlm.nih.gov/Traces/study/?acc=PRJNA659625&o=acc_s%3Aa). In addition, the metadata of the sequencing output can be found in the github webpage https://github.com/PedroHLebre/Hypolith_scriptThe South African National Research Foundation and Antarctica New Zealand.https://academic.oup.com/femsec2021-10-17hj2021BiochemistryGeneticsMicrobiology and Plant Patholog

Islands in the sand: are all hypolithic microbial communities the same?

Hypolithic microbial communities (hypolithons) are complex assemblages of phototrophic and heterotrophic organisms associated with the ventral surfaces of translucent minerals embedded in soil surfaces. Past studies on the assembly, structure and function of hypolithic communities have tended to use composite samples (i.e. bulked hypolithic biomass) with the underlying assumption that samples collected from within a ‘homogeneous’ locality are phylogenetically homogeneous. In this study, we question this assumption by analysing the prokaryote phylogenetic diversity of multiple individual hypolithons: i.e. asking the seemingly simple question of ‘Are all hypolithons the same’? Using 16S rRNA gene-based phylogenetic analysis of hypolithons recovered for a localized moraine region in the Taylor Valley, McMurdo Dry Valleys, Antarctica, we demonstrate that these communities are heterogeneous at very small spatial scales (&amp;lt;5 m). Using null models of phylogenetic turnover, we showed that this heterogeneity between hypolithons is probably due to stochastic effects such as dispersal limitations, which is entirely consistent with the physically isolated nature of the hypolithic communities (‘islands in the sand’) and the almost complete absence of a liquid continuum as a mode of microbial transport between communities