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1. Microbial Diversity and Sulfur Cycling in an Early Earth Analogue: From Ancient Novelty to Modern Commonality

   https://doi.org/10.1128/mbio.00016-22  

   Hahn, C. Ryan ; Farag, Ibrahim F. ; Murphy, Chelsea L. ; Podar, Mircea ; Elshahed, Mostafa S. ; Youssef, Noha H. ( April 2022 , mBio)

   Sousa, Filipa L. ; Schleper, Christa M. (Ed.)

   ABSTRACT Life emerged and diversified in the absence of molecular oxygen. The prevailing anoxia and unique sulfur chemistry in the Paleo-, Meso-, and Neoarchean and early Proterozoic eras may have supported microbial communities that differ from those currently thriving on the earth’s surface. Zodletone spring in southwestern Oklahoma represents a unique habitat where spatial sampling could substitute for geological eras namely, from the anoxic, surficial light-exposed sediments simulating a preoxygenated earth to overlaid water column where air exposure simulates oxygen intrusion during the Neoproterozoic era. We document a remarkably diverse microbial community in the anoxic spring sediments, with 340/516 (65.89%) of genomes recovered in a metagenomic survey belonging to 200 bacterial and archaeal families that were either previously undescribed or that exhibit an extremely rare distribution on the current earth. Such diversity is underpinned by the widespread occurrence of sulfite, thiosulfate, tetrathionate, and sulfur reduction and the paucity of sulfate reduction machineries in these taxa. Hence, these processes greatly expand lineages mediating reductive sulfur-cycling processes in the tree of life. An analysis of the overlaying oxygenated water community demonstrated the development of a significantly less diverse community dominated by well-characterized lineages and a prevalence of oxidative sulfur-cycling processes. Such a transition from ancient novelty to modern commonality underscores the profound impact of the great oxygenation event on the earth’s surficial anoxic community. It also suggests that novel and rare lineages encountered in current anaerobic habitats could represent taxa that once thrived in an anoxic earth but have failed to adapt to earth’s progressive oxygenation. IMPORTANCE Life on earth evolved in an anoxic setting; however, the identity and fate of microorganisms that thrived in a preoxygenated earth are poorly understood. In Zodletone spring, the prevailing geochemical conditions are remarkably similar to conditions prevailing in surficial earth prior to oxygen buildup in the atmosphere. We identify hundreds of previously unknown microbial lineages in the spring and demonstrate that these lineages possess the metabolic machinery to mediate a wide range of reductive sulfur processes, with the capacity to respire sulfite, thiosulfate, sulfur, and tetrathionate, rather than sulfate, which is a reflection of the differences in sulfur-cycling chemistry in ancient versus modern times. Collectively, such patterns strongly suggest that microbial diversity and sulfur-cycling processes in a preoxygenated earth were drastically different from the currently observed patterns and that the Great Oxygenation Event has precipitated the near extinction of a wide range of oxygen-sensitive lineages and significantly altered the microbial reductive sulfur-cycling community on earth. 

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2. Groundwater shapes sediment biogeochemistry and microbial diversity in a submerged Great Lake sinkhole

   https://doi.org/10.1111/gbi.12215  

   Kinsman‐Costello, L. E. ; Sheik, C. S. ; Sheldon, N. D. ; Allen Burton, G. ; Costello, D. M. ; Marcus, D. ; Uyl, P. A. Den ; Dick, G. J. ( September 2016 , Geobiology)

   For a large part of earth's history, cyanobacterial mats thrived in low‐oxygen conditions, yet our understanding of their ecological functioning is limited. Extant cyanobacterial mats provide windows into the putative functioning of ancient ecosystems, and they continue to mediate biogeochemical transformations and nutrient transport across the sediment–water interface in modern ecosystems. The structure and function of benthic mats are shaped by biogeochemical processes in underlying sediments. A modern cyanobacterial mat system in a submerged sinkhole of Lake Huron (LH) provides a unique opportunity to explore such sediment–mat interactions. In the Middle Island Sinkhole (MIS), seeping groundwater establishes a low‐oxygen, sulfidic environment in which a microbial mat dominated byPhormidiumandPlanktothrixthat is capable of both anoxygenic and oxygenic photosynthesis, as well as chemosynthesis, thrives. We explored the coupled microbial community composition and biogeochemical functioning of organic‐rich, sulfidic sediments underlying the surface mat. Microbial communities were diverse and vertically stratified to 12 cm sediment depth. In contrast to previous studies, which used low‐throughput or shotgun metagenomic approaches, our high‐throughput 16SrRNAgene sequencing approach revealed extensive diversity. This diversity was present within microbial groups, including putative sulfate‐reducing taxa ofDeltaproteobacteria, some of which exhibited differential abundance patterns in the mats and with depth in the underlying sediments. The biological and geochemical conditions in theMISwere distinctly different from those in typicalLHsediments of comparable depth. We found evidence for active cycling of sulfur, methane, and nutrients leading to high concentrations of sulfide, ammonium, and phosphorus in sediments underlying cyanobacterial mats. Indicators of nutrient availability were significantly related toMISmicrobial community composition, whileLHcommunities were also shaped by indicators of subsurface groundwater influence. These results show that interactions between the mats and sediments are crucial for sustaining this hot spot of biological diversity and biogeochemical cycling.

    

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3. Elevational Constraints on the Composition and Genomic Attributes of Microbial Communities in Antarctic Soils

   https://doi.org/10.1128/msystems.01330-21  

   Dragone, Nicholas B. ; Henley, Jessica B. ; Holland-Moritz, Hannah ; Diaz, Melisa ; Hogg, Ian D. ; Lyons, W. Berry ; Wall, Diana H. ; Adams, Byron J. ; Fierer, Noah ( February 2022 , mSystems)

   Mackelprang, Rachel (Ed.)

   ABSTRACT The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. 

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4. Lipid Biomarkers From Microbial Mats on the McMurdo Ice Shelf, Antarctica: Signatures for Life in the Cryosphere

   https://doi.org/10.3389/fmicb.2022.903621  

   Evans, Thomas W. ; Kalambokidis, Maria J. ; Jungblut, Anne D. ; Millar, Jasmin L. ; Bauersachs, Thorsten ; Grotheer, Hendrik ; Mackey, Tyler J. ; Hawes, Ian ; Summons, Roger E. ( June 2022 , Frontiers in Microbiology)

   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. 

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5. Variations and gradients between methane seep and off-seep microbial communities in a submarine canyon system in the Northeast Pacific

   https://doi.org/10.7717/peerj.15119  

   Cummings, Susie ; Ardor Bellucci, Lila M. ; Seabrook, Sarah ; Raineault, Nicole A. ; McPhail, Kerry L. ; Thurber, Andrew R. ( January 2023 , PeerJ)

   Methane seeps are highly abundant marine habitats that contribute sources of chemosynthetic primary production to marine ecosystems. Seeps also factor into the global budget of methane, a potent greenhouse gas. Because of these factors, methane seeps influence not only local ocean ecology, but also biogeochemical cycles on a greater scale. Methane seeps host specialized microbial communities that vary significantly based on geography, seep gross morphology, biogeochemistry, and a diversity of other ecological factors including cross-domain species interactions. In this study, we collected sediment cores from six seep and non-seep locations from Grays and Quinault Canyons (46–47°N) off Washington State, USA, as well as one non-seep site off the coast of Oregon, USA (45°N) to quantify the scale of seep influence on biodiversity within marine habitats. These samples were profiled using 16S rRNA gene sequencing. Predicted gene functions were generated using the program PICRUSt2, and the community composition and predicted functions were compared among samples. The microbial communities at seeps varied by seep morphology and habitat, whereas the microbial communities at non-seep sites varied by water depth. Microbial community composition and predicted gene function clearly transitioned from on-seep to off-seep in samples collected from transects moving away from seeps, with a clear ecotone and high diversity where methane-fueled habitats transition into the non-seep deep sea. Our work demonstrates the microbial and metabolic sphere of influence that extends outwards from methane seep habitats. 

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