TY - JOUR T1 - Lipid biomarkers from microbial mats on the McMurdo Ice Shelf, Antarctica: Signatures for life in the cryosphere JF - Frontiers in Microbiology Y1 - 2022 A1 - Evans, Thomas W. A1 - Kalambokidis, Maria J. A1 - Jungblut, Anne D. A1 - Millar, Jasmin L. A1 - Bauersachs, Thorsten A1 - Grotheer, Hendrik A1 - Mackey, Tyler J. A1 - Ian Hawes A1 - Summons, Roger E. KW - Antarctica KW - bacteriohopanepolyol KW - cyanobacteria KW - heterocyte glycolipids KW - homeoviscous adaptation KW - intact polar lipid KW - microbial mats AB -

Persistent cold temperatures, a paucity of nutrients, freeze-thaw cycles, and the strongly seasonal light regime make Antarctica one of Earth’s least hospitable surface environments for complex life. Cyanobacteria, however, are well-adapted to such conditions and are often the dominant primary producers in Antarctic inland water environments. In particular, the network of meltwater ponds on the ‘dirty ice’ of the McMurdo Ice Shelf is an ecosystem with extensive cyanobacteria-dominated microbial mat accumulations. This study investigated intact polar lipids (IPLs), heterocyte glycolipids (HGs), and bacteriohopanepolyols (BHPs) in combination with 16S and 18S rRNA gene diversity in microbial mats of twelve ponds in this unique polar ecosystem. To constrain the effects of nutrient availability, temperature and freeze-thaw cycles on the lipid membrane composition, lipids were compared to stromatolite-forming cyanobacterial mats from ice-covered lakes in the McMurdo Dry Valleys as well as from (sub)tropical regions and hot springs. The 16S rRNA gene compositions of the McMurdo Ice Shelf mats confirm the dominance of Cyanobacteria and Proteobacteria while the 18S rRNA gene composition indicates the presence of Ochrophyta, Chlorophyta, Ciliophora, and other microfauna. IPL analyses revealed a predominantly bacterial community in the meltwater ponds, with archaeal lipids being barely detectable. IPLs are dominated by glycolipids and phospholipids, followed by aminolipids. The high abundance of sugar-bound lipids accords with a predominance of cyanobacterial primary producers. The phosphate-limited samples from the (sub)tropical, hot spring, and Lake Vanda sites revealed a higher abundance of aminolipids compared to those of the nitrogen-limited meltwater ponds, affirming the direct affects that N and P availability have on IPL compositions. The high abundance of polyunsaturated IPLs in the Antarctic microbial mats suggests that these lipids provide an important mechanism to maintain membrane fluidity in cold environments. High abundances of HG keto-ols and HG keto-diols, produced by heterocytous cyanobacteria, further support these findings and reveal a unique distribution compared to those from warmer climates.

VL - 13 UR - https://www.frontiersin.org/articles/10.3389/fmicb.2022.903621/full JO - Front. Microbiol. ER - TY - JOUR T1 - Metabolic capacity of the Antarctic cyanobacterium Phormidium pseudopriestleyi that sustains oxygenic photosynthesis in the presence of hydrogen sulfide JF - Genes Y1 - 2021 A1 - Lumian, Jessica E. A1 - Jungblut, Anne D. A1 - Dillon, Megan L. A1 - Hawes, Ian A1 - Peter T. Doran A1 - Mackey, Tyler J. A1 - Dick, Gregory J. A1 - Grettenberger, Christen L. A1 - Sumner, Dawn Y. AB -

Sulfide inhibits oxygenic photosynthesis by blocking electron transfer between H2O and the oxygen-evolving complex in the D1 protein of Photosystem II. The ability of cyanobacteria to counter this effect has implications for understanding the productivity of benthic microbial mats in sulfidic environments throughout Earth history. In Lake Fryxell, Antarctica, the benthic, filamentous cyanobacterium Phormidium pseudopriestleyi creates a 1–2 mm thick layer of 50 µmol L−1 O2 in otherwise sulfidic water, demonstrating that it sustains oxygenic photosynthesis in the presence of sulfide. A metagenome-assembled genome of P. pseudopriestleyi indicates a genetic capacity for oxygenic photosynthesis, including multiple copies of psbA (encoding the D1 protein of Photosystem II), and anoxygenic photosynthesis with a copy of sqr (encoding the sulfide quinone reductase protein that oxidizes sulfide). The genomic content of P. pseudopriestleyi is consistent with sulfide tolerance mechanisms including increasing psbA expression or directly oxidizing sulfide with sulfide quinone reductase. However, the ability of the organism to reduce Photosystem I via sulfide quinone reductase while Photosystem II is sulfide-inhibited, thereby performing anoxygenic photosynthesis in the presence of sulfide, has yet to be demonstrated. 

VL - 12 UR - https://www.mdpi.com/2073-4425/12/3/426 IS - 3 ER - TY - JOUR T1 - Energetic and environmental constraints on the community structure of benthic microbial mats in Lake Fryxell, Antarctica JF - FEMS Microbiology Ecology Y1 - 2020 A1 - Dillon, Megan L. A1 - Ian Hawes A1 - Jungblut, Anne D. A1 - Mackey, Tyler J. A1 - Eisen, Jonathan A. A1 - Peter T. Doran A1 - Sumner, Dawn Y. KW - Antarctica KW - energy KW - Lake Fryxell KW - microbial mat KW - Oxygen KW - Photosynthetically Active Radiation AB -

Ecological communities are regulated by the flow of energy through environments. Energy flow is typically limited by access to photosynthetically active radiation (PAR) and oxygen concentration (O2). The microbial mats growing on the bottom of Lake Fryxell, Antarctica, have well-defined environmental gradients in PAR and (O2). We analyzed the metagenomes of layers from these microbial mats to test the extent to which access to oxygen and light controls community structure. We found variation in the diversity and relative abundances of Archaea, Bacteria and Eukaryotes across three (O2) and PAR conditions: high (O2) and maximum PAR, variable (O2) with lower maximum PAR, and low (O2) and maximum PAR. We found distinct communities structured by the optimization of energy use on a millimeter-scale across these conditions. In mat layers where (O2) was saturated, PAR structured the community. In contrast, (O2) positively correlated with diversity and affected the distribution of dominant populations across the three habitats, suggesting that meter-scale diversity is structured by energy availability. Microbial communities changed across covarying gradients of PAR and (O2). The comprehensive metagenomic analysis suggests that the benthic microbial communities in Lake Fryxell are structured by energy flow across both meter- and millimeter-scales.

VL - 96 UR - https://academic.oup.com/femsec/article/96/2/fiz207/5697196 IS - 2 ER - TY - JOUR T1 - Environmental control on the distribution of metabolic strategies of benthic microbial mats in Lake Fryxell, Antarctica JF - PLoS ONE Y1 - 2020 A1 - Dillon, Megan L. A1 - Hawes, Ian A1 - Jungblut, Anne D. A1 - Mackey, Tyler J. A1 - Eisen, Jonathan A. A1 - Peter T. Doran A1 - Sumner, Dawn Y. AB -

Ecological theories posit that heterogeneity in environmental conditions greatly affects community structure and function. However, the degree to which ecological theory developed using plant- and animal-dominated systems applies to microbiomes is unclear. Investigating the metabolic strategies found in microbiomes are particularly informative for testing the universality of ecological theories because microorganisms have far wider metabolic capacity than plants and animals. We used metagenomic analyses to explore the relationships between the energy and physicochemical gradients in Lake Fryxell and the metabolic capacity of its benthic microbiome. Statistical analysis of the relative abundance of metabolic marker genes and gene family diversity shows that oxygenic photosynthesis, carbon fixation, and flavin-based electron bifurcation differentiate mats growing in different environmental conditions. The pattern of gene family diversity points to the likely importance of temporal environmental heterogeneity in addition to resource gradients. Overall, we found that the environmental heterogeneity of photosynthetically active radiation (PAR) and oxygen concentration ([O2]) in Lake Fryxell provide the framework by which metabolic diversity and composition of the community is structured, in accordance with its phylogenetic structure. The organization of the resulting microbial ecosystems are consistent with the maximum power principle and the species sorting model.

VL - 15 UR - https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0231053 IS - 4 ER - TY - CHAP T1 - Complex Structure but Simple Function in Microbial Mats from Antarctic Lakes T2 - The Structure and Function of Aquatic Microbial Communities Y1 - 2019 A1 - Ian Hawes A1 - Sumner, Dawn Y. A1 - Jungblut, Anne D. ED - Hurst, Christon J. KW - biofilm KW - microbial ecology KW - microbial structures KW - self-organising structures KW - stromatolite AB -

Microbial mats growing under the permanent ice cover of Antarctic lakes occupy an exceptionally low-disturbance regime. Constant temperature, the absence of bioturbation or physical disturbance from wind action or ice formation allow mats to accumulate, as annual growth layers, over many decades or even centuries. In so doing they often assume decimetre scale, three-dimensional morphologies such as elaborate pinnacle structures and conical mounds. Here we combine existing and new information to describe microbial structures in three Antarctic lakes—simple prostrate mats in Lake Hoare, emergent cones in Lake Untersee and elaborate pinnacles in Lake Vanda. We attempt to determine whether structures emerge simply from uncoordinated organism-environment interactions or whether they represent an example of “emergent complexity”, within which some degree of self-organisation occurs to confer a holistic functional advantage to component organisms. While some holistic advantages were evident from the structures—the increase in surface area allows greater biomass and overall productivity and nutrient exchange with overlying water—the structures could also be understood in terms of potential interactions between individuals, their orientation and their environment. The data lack strong evidence of coordinated behaviour directed towards holistic advantages to the structure, though hints of coordinated behaviour are present as non-random distributions of structural elements. The great size of microbial structures in Antarctic lakes, and their relatively simple community composition, makes them excellent models for more focused research on microbial cooperation.

JF - The Structure and Function of Aquatic Microbial Communities PB - Springer International Publishing CY - Cham SN - 978-3-030-16775-2 UR - https://link.springer.com/chapter/10.1007/978-3-030-16775-2_4 ER - TY - JOUR T1 - Environmental controls on bacteriohopanepolyol profiles of benthic microbial mats from Lake Fryxell, Antarctica JF - Geobiology Y1 - 2019 A1 - Matys, Emily D. A1 - Mackey, Tyler J. A1 - Grettenberger, Christen A1 - Mueller, Elliott A1 - Jungblut, Anne D. A1 - Sumner, Dawn Y. A1 - Ian Hawes A1 - Summons, Roger E. KW - anammox KW - bacteriohopanepolyol KW - bacteriohopanetetrol isomer KW - biomarker KW - McMurdo Dry Valleys AB -

Bacteriohopanepolyols (BHPs) are pentacyclic triterpenoid lipids that contribute to the structural integrity and physiology of some bacteria. Because some BHPs originate from specific classes of bacteria, BHPs have potential as taxonomically and environmentally diagnostic biomarkers. For example, a stereoisomer of bacteriohopanetetrol (informally BHT II) has been associated with anaerobic ammonium oxidation (anammox) bacteria and suboxic to anoxic marine environments where anammox is active. As a result, the detection of BHT II in the sedimentary record and fluctuations in the relative abundance of BHT II may inform reconstructions of nitrogen cycling and ocean redox changes through the geological record. However, there are uncertainties concerning the sources of BHT II and whether or not BHT II is produced in abundance in non‐marine environments, both of which are pertinent to interpretations of BHT II signatures in sediments. To address these questions, we investigate the BHP composition of benthic microbial mats from Lake Fryxell, Antarctica. Lake Fryxell is a perennially ice‐covered lake with a sharp oxycline in a density‐stabilized water column. We describe the diversity and abundance of BHPs in benthic microbial mats across a transect from oxic to anoxic conditions. Generally, BHP abundances and diversity vary with the morphologies of microbial mats, which were previously shown to reflect local environmental conditions, such as irradiance and oxygen and sulfide concentrations. BHT II was identified in mats that exist within oxic to anoxic portions of the lake. However, anammox bacteria have yet to be identified in Lake Fryxell. We examine our results in the context of BHPs as biomarkers in modern and ancient environments.

UR - https://onlinelibrary.wiley.com/doi/full/10.1111/gbi.12353 ER - TY - JOUR T1 - Growth dynamics of a laminated microbial mat in response to variable irradiance in an Antarctic lake JF - Freshwater Biology Y1 - 2016 A1 - Ian Hawes A1 - Jungblut, Anne D. A1 - Maciek K. Obryk A1 - Peter T. Doran AB -
  1. Laminated microbial mats are important ecosystem components of perennially ice-covered Antarctic dry valley lakes. In order to understand better their response to changing environment, we made observations and carried out a manipulation experiment to determine their response to variations in irradiance in Lake Hoare (77°38′ S, 162°53′ E).
  2. Ice transparency was the most variable parameter that affected benthic light dose, both spatially and between years. Patterns of lamina accrual corresponded to irradiance history, with laminae that were initiated in high transmission years thicker than those from low transmission years.
  3. A shading experiment confirmed that accrual of lamina thickness, calcite precipitation and ash-free dry mass were determined by irradiance, but photosynthetic biomass and phototrophic species composition were less affected.
  4. Buried laminae decomposed only slowly over time, with potentially viable phototrophs many laminae down into the microbial mat. Decay rate increased only slightly with shading.
  5. We conclude that the microbial mats in Lake Hoare are characterised by remarkable stability, with slow accumulation rates and turnover of biomass over time. Photosynthetic biomass and species composition appeared to be stable across long time periods, with interannual variation in lamination pattern due to differential accumulation of extracellular polysaccharide and representing the visible expression of annual growth conditions.
VL - 61 UR - http://doi.wiley.com/10.1111/fwb.12715 IS - 4 JO - Freshw Biol ER - TY - JOUR T1 - Microbial Mat Communities along an Oxygen Gradient in a Perennially Ice-Covered Antarctic Lake JF - Applied and Environmental Microbiology Y1 - 2016 A1 - Jungblut, Anne D. A1 - Ian Hawes A1 - Mackey, Tyler J. A1 - Krusor, Megan A1 - Peter T. Doran A1 - Sumner, Dawn Y. A1 - Eisen, Jonathan A. A1 - Hillman, Colin A1 - Goroncy, Alexander K. ED - Stams, A. J. VL - 82 UR - http://aem.asm.org/lookup/doi/10.1128/AEM.02699-15 IS - 2 JO - Appl. Environ. Microbiol. ER - TY - JOUR T1 - Antarctic microbial mats: A modern analog for Archean lacustrine oxygen oases JF - Geology Y1 - 2015 A1 - Sumner, Dawn Y. A1 - Ian Hawes A1 - Mackey, Tyler J. A1 - Jungblut, Anne D. A1 - Peter T. Doran AB -

The evolution of oxygenic photosynthesis was the most important geochemical event in

Earth history, causing the Great Oxidation Event (GOE) ~2.4 b.y. ago. However, evidence is mixed as to whether O2 production occurred locally as much as 2.8 b.y. ago, creating O2 oases, or initiated just prior to the GOE. The biogeochemical dynamics of possible O2 oases have been poorly constrained due to the absence of modern analogs. However, cyanobacteria in microbial mats in a perennially anoxic region of Lake Fryxell, Antarctica, create a 1–2 mm O2-containing layer in the upper mat during summer, providing the first known modern analog for formation of benthic O2 oases. In Lake Fryxell, benthic cyanobacteria are present below the oxycline in the lake. Mat photosynthesis rates were slow due to low photon flux rate (1–2 μmol m-2 s-1) under thick ice cover, but photosynthetic O2 production was sufficient to sustain up to 50 μmol O2 L-1, sandwiched between anoxic overlying water and anoxic sedi- ments. We hypothesize that Archean cyanobacteria could have similarly created O2 oases in benthic mats prior to the GOE. Analogous mats may have been at least partly responsible for geological evidence of oxidative weathering prior to the GOE, and habitats such as Lake Fryxell provide natural laboratories where the impact of benthic O2 oases on biogeochemical signatures can be investigated. 

 

UR - http://geology.gsapubs.org/lookup/doi/10.1130/G36966.1 JO - Geology ER - TY - JOUR T1 - Cyanobacterial diversity in benthic mats of the McMurdo Dry Valley lakes, Antarctica JF - Polar Biology Y1 - 2015 A1 - Zhang, L. A1 - Jungblut, Anne D. A1 - Ian Hawes A1 - Dale T. Andersen A1 - Sumner, Dawn Y. A1 - Mackey, Tyler J. AB -
Perennially ice-covered, meromictic lakes in the McMurdo Dry Valleys, Antarctica, are useful models to study the relationship between cyanobacterial and environmental variables. They have rich benthic cyanobacterial mat accumulations and stable stratification of physical and chemical conditions. Here, we evaluated cyanobacteria from benthic mats from multiple depths in three geographically separated ice-covered lakes, Lakes Vanda, Hoare and Joyce, using 16S rRNA gene clone libraries. We identified 19 ribotypes, mostly Oscillatoriales and several
Chroococcales, as well as potentially novel cyanobacterial ribotypes. The majority of ribotype diversity was shared between lakes, and only a weak relationship between ribotype community structure and environmental variables was evident. Multivariate analysis of all lake–depth combinations implied that photosynthetically active radiation, dissolved reactive phosphorus and conductivity were potentially important for shaping benthic communities in McMurdo Dry Valley lakes. Cyanobacterial-specific pigment signature analysis by high-performance liquid chromatography
showed that the cyanobacterial communities responded to light conditions similarly, irrespective of community composition. The results imply a capability within a suite of cyanobacteria to colonise, adapt and grow across broad environmental ranges and geographic space, and such adaptability may provide a high degree of community resistance and resilience to future climate-driven environmental change in Antarctic terrestrial aquatic
ecosystems.
VL - 38 UR - http://link.springer.com/10.1007/s00300-015-1669-0http://link.springer.com/content/pdf/10.1007/s00300-015-1669-0 IS - 8 JO - Polar Biol ER -