02559nas a2200301 4500008004100000245008000041210006900121260001200190300001200202490000700214520166000221653001501881653001601896653002901912653001801941653001201959100002901971700001802000700002202018700002002040700002202060700001202082700001602094700002602110700002102136700003302157856006702190 2024 eng d00aSentinel protist taxa of the McMurdo Dry Valley lakes, Antarctica: A review0 aSentinel protist taxa of the McMurdo Dry Valley lakes Antarctica c03/2024 a13234720 v123 a

High-latitude meromictic lakes such as those in the Antarctic McMurdo Dry Valleys (MDV) harbor aquatic ecosystems dominated by the microbial loop. Within this habitat, which is limited year-round by light and nutrients, protists, or single celled eukaryotes, play outsized roles in the food web as the dominant primary producers and the apex predators. Thus, the MDV lake ecosystem represents an ideal system to study the role of sentinel protist taxa in carbon and nutrient cycling. The perennially ice-covered lakes are part of the McMurdo Long Term Ecological Research (McM LTER; mcmlter.org) established in 1993. In this review we will highlight the diversity and trophic roles of the MDV lake protist community and compare environmental factors driving spatiotemporal patterns in key protist taxa in two lakes within the McM LTER, Lakes Bonney and Fryxell. We will then discuss lessons learned from manipulated experiments on the impact of current and future climate-driven environmental change on sensitive protist taxa. Last, we will integrate knowledge gained from 25 years of lab-controlled experiments on key photosynthetic protists to extend our understanding of the function of these extremophiles within the MDV aquatic food webs. Our research group has studied the distribution and function of the MDV microbial community for nearly two decades, training the next generation of scientists to tackle future problems of these globally significant microbes. This review article will also highlight early career scientists who have contributed to this body of work and represent the future of scientific understanding in the Anthropocene.

10aAntarctica10aDisturbance10aMcMurdo Dry Valley lakes10aphytoplankton10aprotist1 aMorgan-Kiss, Rachael, M.1 aPopson, Devon1 aPereira, Rochelle1 aDolhi-Binder, J1 aTeufel, Amber, G.1 aLi, Wei1 aKalra, Isha1 aSherwell, Shasten, S.1 aReynebeau, Emily1 aTakacs-Vesbach, Cristina, D. uhttps://www.frontiersin.org/articles/10.3389/fevo.2024.132347202039nas a2200169 4500008004100000245013000041210007100171260001200242520142300254100002601677700001601703700001201719700002401731700002101755700002901776856006401805 2022 eng d00aAntarctic lake phytoplankton and bacteria from near‐surface waters exhibit high sensitivity to climate‐driven disturbance0 aAntarctic lake phytoplankton and bacteria from near‐surface wate c07/20223 a

The McMurdo Dry Valleys (MDVs), Antarctica, represent a cold, desert ecosystem poised on the threshold of melting and freezing water. The MDVs have experienced dramatic signs of climatic change, most notably a warm austral summer in 2001–2002 that caused widespread flooding, partial ice cover loss and lake level rise. To understand the impact of these climatic disturbances on lake microbial communities, we simulated lake level rise and ice-cover loss by transplanting dialysis-bagged communities from selected depths to other locations in the water column or to an open water perimeter moat. Bacteria and eukaryote communities residing in the surface waters (5 m) exhibited shifts in community composition when exposed to either disturbance, while microbial communities from below the surface were largely unaffected by the transplant. We also observed an accumulation of labile dissolved organic carbon in the transplanted surface communities. In addition, there were taxa-specific sensitivities: cryptophytes and Actinobacteria were highly sensitive particularly to the moat transplant, while chlorophytes and several bacterial taxa increased in relative abundance or were unaffected. Our results reveal that future climate-driven disturbances will likely undermine the stability and productivity of MDV lake phytoplankton and bacterial communities in the surface waters of this extreme environment.

1 aSherwell, Shasten, S.1 aKalra, Isha1 aLi, Wei1 aMcKnight, Diane, M.1 aPriscu, John, C.1 aMorgan-Kiss, Rachael, M. uhttps://onlinelibrary.wiley.com/doi/10.1111/1462-2920.1611302431nas a2200277 4500008004100000022001300041245008500054210006900139260001200208300001100220490000800231520163400239653001501873653001301888653001401901653001901915653001901934653001901953100001401972700001201986700002501998700002102023700001702044700001602061856007602077 2022 eng d a0048969700aOrganic matter distribution in the icy environments of Taylor Valley, Antarctica0 aOrganic matter distribution in the icy environments of Taylor Va c10/2022 a1566390 v8413 a

Glaciers can accumulate and release organic matter affecting the structure and function of associated terrestrial and aquatic ecosystems. We analyzed 18 ice cores collected from six locations in Taylor Valley (McMurdo Dry Valleys), Antarctica to determine the spatial abundance and quality of organic matter, and the spatial distribution of bacterial density and community structure from the terminus of the Taylor Glacier to the coast (McMurdo Sound). Our results showed that dissolved and particulate organic carbon (DOC and POC) concentrations in the ice core samples increased from the Taylor Glacier to McMurdo Sound, a pattern also shown by bacterial cell density. Fluorescence Excitation Emission Matrices Spectroscopy (EEMs) and multivariate parallel factor (PARAFAC) modeling identified one humic-like (C1) and one protein-like (C2) component in ice cores whose fluorescent intensities all increased from the Polar Plateau to the coast. The fluorescence index showed that the bioavailability of dissolved organic matter (DOM) also decreased from the Polar Plateau to the coast. Partial least squares path modeling analysis revealed that bacterial abundance was the main positive biotic factor influencing both the quantity and quality of organic matter. Marine aerosol influenced the spatial distribution of DOC more than katabatic winds in the ice cores. Certain bacterial taxa showed significant correlations with DOC and POC concentrations. Collectively, our results show the tight connectivity among organic matter spatial distribution, bacterial abundance and meteorology in the McMurdo Dry Valley ecosystem.

10aAntarctica10abacteria10aice cores10akatabatic wind10amarine aerosol10aorganic matter1 aGuo, Bixi1 aLi, Wei1 aSantibáñez, Pamela1 aPriscu, John, C.1 aLiu, Yongqin1 aLiu, Keshao uhttps://www.sciencedirect.com/science/article/abs/pii/S004896972203736602448nas a2200217 4500008004100000245010000041210006900141260001200210490000700222520174400229100001201973700001901985700002702004700002102031700001602052700001702068700002902085700002302114700002102137856007202158 2020 eng d00aMethane production in the oxygenated water column of a perennially ice‐covered Antarctic lake0 aMethane production in the oxygenated water column of a perennial c01/20200 v653 a

Aerobic methane production in aquatic ecosystems impacts the global atmospheric budget of methane, but the extent, mechanism, and taxa responsible for producing this greenhouse gas are not fully understood. Lake Bonney (LB), a perennially ice‐covered Antarctic lake, has cold hypersaline waters underlying an oxygenated freshwater layer. We present temporal methane concentration profiles in LB indicating methane production in the oxygenated (> 200% air saturation) water. Experiments amended with methylphosphonate (MPn) yielded methane generation, suggesting in situ methanogenesis via the carbon‐phosphorus (C‐P) lyase pathway. Enrichment cultures from the lake were used to isolate five bacterial strains capable of generating methane when supplied with MPn as the sole P source. Based on 16S rRNA gene sequencing, the isolates belong to the Proteobacteria (closely related to Marinomonas, Hoeflea, and Marinobacter genera) and Bacteroidetes (Algoriphagus genus). 16S rRNA metagenomic sequencing confirms the presence of these taxa in LB. None of the isolated species were reported to be capable to produce methane. In addition, orthologs of the phosphoenolpyruvate mutase gene (PepM) and methylphosphonate synthase (MPnS), enzymes involved in phosphonate and MPn biosynthesis, were widely spread in the LB shotgun metagenomic libraries; genes related to C‐P lyase pathways (phn gene clusters) were also abundant. 16S rRNA and mcrA genes of anaerobic methanogens were absent in both 16S rRNA and metagenomics libraries. These data reveal that in situ aerobic biological methane production is likely a significant source of methane in LB.

1 aLi, Wei1 aDore, John, E.1 aSteigmeyer, August, J.1 aCho, Yong‐Joon1 aKim, Ok-Sun1 aLiu, Yongqin1 aMorgan-Kiss, Rachael, M.1 aSkidmore, Mark, L.1 aPriscu, John, C. uhttps://aslopubs.onlinelibrary.wiley.com/doi/full/10.1002/lno.1125702684nas a2200265 4500008004100000022001400041245014900055210006900204260001200273490000600285520185300291653001502144653002502159653000902184653001802193653001702211100001502228700001802243700001602261700001202277700001402289700002102303700002902324856006502353 2019 eng d a0166-859500aThe Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of photosystem I in response to iron0 aAntarctic psychrophiles iChlamydomonasi spp UWO241 and ICEMDV ex c02/20190 v93 a

Chlamydomonas sp. UWO241 is a psychrophilic alga isolated from the deep photic zone of a perennially ice-covered Antarctic lake (east lobe Lake Bonney, ELB). Past studies have shown that C. sp. UWO241 exhibits constitutive downregulation of photosystem I (PSI) and high rates of PSI-associated cyclic electron flow (CEF). Iron levels in ELB are in the nanomolar range leading us to hypothesize that the unusual PSI phenotype of C. sp. UWO241 could be a response to chronic Fe-deficiency. We studied the impact of Fe availability in C. sp. UWO241, a mesophile, C. reinhardtii SAG11-32c, as well as a psychrophile isolated from the shallow photic zone of ELB, Chlamydomonas sp. ICE-MDV. Under Fe-deficiency, PsaA abundance and levels of photooxidizable P700 (ΔA820/A820) were reduced in both psychrophiles relative to the mesophile. Upon increasing Fe, C. sp. ICE-MDV and C. reinhardtii exhibited restoration of PSI function, while C. sp. UWO241 exhibited only moderate changes in PSI activity and lacked almost all LHCI proteins. Relative to Fe-excess conditions (200 μM Fe2+), C. sp. UWO241 grown in 18 μM Fe2+ exhibited downregulation of light harvesting and photosystem core proteins, as well as upregulation of a bestrophin-like anion channel protein and two CEF-associated proteins (NdsS, PGL1). Key enzymes of starch synthesis and shikimate biosynthesis were also upregulated. We conclude that in response to variable Fe availability, the psychrophile C. sp. UWO241 exhibits physiological plasticity which includes restructuring of the photo-chemical apparatus, increased PSI-associated CEF, and shifts in downstream carbon metabolism toward storage carbon and secondary stress metabolites.

10aAntarctica10aCyclic electron flow10aIron10aPhotosystem I10aPsychrophile1 aCook, Greg1 aTeufel, Amber1 aKalra, Isha1 aLi, Wei1 aWang, Xin1 aPriscu, John, C.1 aMorgan-Kiss, Rachael, M. uhttps://link.springer.com/article/10.1007/s11120-019-00621-002573nas a2200265 4500008004100000022001400041245010400055210006900159260001200228300001400240490000700254520177600261653002002037653002102057653001502078653001702093653002402110653001202134653002502146100001202171700002002183700001602203700002902219856005902248 2019 eng d a0948-305500aDrivers of protistan community autotrophy and heterotrophy in chemically stratified Antarctic lakes0 aDrivers of protistan community autotrophy and heterotrophy in ch c01/2019 a225 - 2390 v823 a

Single-celled, eukaryotic microorganisms, known as protists, are responsible for 2 important, yet opposing, metabolic activities within aquatic food webs. They are major primary producers and highly active predators in marine and fresh water systems. While genomics has accelerated in recent years for this taxonomically diverse group, our understanding of the metabolic capabilities of most protists remains limited. It is also poorly understood how protist trophic mode is affected by biotic and abiotic factors, and therefore it is difficult to predict how events such as global climate change will affect the balance between autotrophic and heterotrophic activities in protist communities. To address open questions regarding how protist metabolic versatility is influenced by their environment, we characterized the potential for carbon fixation versus organic carbon degradation using enzymatic assays (RubisCO and β-D-glucosaminidase, respectively) within the water columns of ice-covered lakes in McMurdo Dry Valleys (MDV), Antarctica. Steep physical and chemical gradients in the water columns, microorganism domination and minimal allochthonous inputs makes the MDV lakes uniquely suited to investigate environment-microbe interactions. Spatial trends in RubisCO and β-D-glucosaminidase activities were lake-specific and vertically stratified within the water columns. Moreover, bottom-up drivers controlling the activity of C-fixation vs. organic C-degradation among the MDV protist communities were distinct between the upper photic vs. the deep, aphotic zones. We conclude that differential controls over major C-cycling enzymes have important implications on the influence of environmental change on the carbon and nutrient cycles in the MDV lakes.

10aAntarctic lakes10aAquatic protists10aAutotrophy10aHeterotrophy10aMcMurdo Dry Valleys10aRubisCO10aβ-D-glucosaminidase1 aLi, Wei1 aDolhi-Binder, J1 aCariani, ZE1 aMorgan-Kiss, Rachael, M. uhttps://www.int-res.com/abstracts/ame/v82/n3/p225-239/02372nas a2200193 4500008004100000245016100041210006900202260001200271490000700283520165600290653002101946653002601967653002701993653001702020653002902037100001202066700002902078856007102107 2019 eng d00aInfluence of environmental drivers and potential interactions on the distribution of microbial communities from three permanently stratified Antarctic lakes0 aInfluence of environmental drivers and potential interactions on c05/20190 v103 a

The McMurdo Dry Valley (MDV) lakes represent unique habitats in the microbial world. Perennial ice covers protect liquid water columns from either significant allochthonous inputs or seasonal mixing, resulting in centuries of stable biogeochemistry. Extreme environmental conditions including low seasonal photosynthetically active radiation (PAR), near freezing temperatures, and oligotrophy have precluded higher trophic levels from the food webs. Despite these limitations, diverse microbial life flourishes in the stratified water columns, including Archaea, bacteria, fungi, protists, and viruses. While a few recent studies have applied next generation sequencing, a thorough understanding of the MDV lake microbial diversity and community structure is currently lacking. Here we used Illumina MiSeq sequencing of the 16S and 18S rRNA genes combined with a microscopic survey of key eukaryotes to compare the community structure and potential interactions among the bacterial and eukaryal communities within the water columns of Lakes Bonney (east and west lobes, ELB, and WLB, respectively) and Fryxell (FRX). Communities were distinct between the upper, oxic layers and the dark, anoxic waters, particularly among the bacterial communities residing in WLB and FRX. Both eukaryal and bacterial community structure was influenced by different biogeochemical parameters in the oxic and anoxic zones. Bacteria formed complex interaction networks which were lake-specific. Several eukaryotes exhibit potential interactions with bacteria in ELB and WLB, while interactions between these groups in the more productive FRX were relatively rare.

10aAquatic protists10aenvironmental drivers10aheterotrophic bacteria10ainteractions10aMcMurdo Dry Valley lakes1 aLi, Wei1 aMorgan-Kiss, Rachael, M. uhttps://www.frontiersin.org/articles/10.3389/fmicb.2019.01067/full02691nas a2200229 4500008004100000022001400041245015500055210006900210260001200279490000700291520189400298653003402192653001902226653002402245653002202269653002302291100002202314700001202336700002002348700002902368856006402397 2017 eng d a0722-406000aImpact of nitrogen and phosphorus on phytoplankton production and bacterial community structure in two stratified Antarctic lakes: a bioassay approach0 aImpact of nitrogen and phosphorus on phytoplankton production an c05/20170 v403 a

Arctic, Antarctic, and alpine ecosystems are recognized as sensors and sentinels of global change. As a consequence of their high sensitivity to minor climatic perturbations, permanently ice-covered lakes located in the McMurdo Dry Valleys (MDV), Antarctica, represent end members in the global network of inland bodies of water. Episodic climatic events in the form of increased summer glacial melt result in inputs of organic sediment and nutrients from glacial streams to these closed basins. Phytoplankton communities residing in the oligotrophic water columns are highly responsive to pulses in nutrient availability; however, there is a lack of understanding on whether specific phytoplankton groups are more competitive during a summer flood event and how shifts in the phytoplankton community may influence heterotrophic bacteria. A bioassay approach in 3-l bottles was used to investigate the influence of inorganic nitrogen and phosphorus availability on planktonic communities from the oligotrophic upper waters of two chemically distinct MDV lakes (Lakes Bonney and Fryxell) which differ in their external inputs and water column N/P stoichiometry. While microbial community responses varied between lakes and were nutrient-dependent, stimulation of phytoplankton biomass and productivity across all treatments was strongly linked with increased abundance of a single phytoplankton phylum (Chlorophyta). Despite stimulation of phytoplankton growth, primary and bacterial productivity was generally uncoupled; however, shifts in bacterial community diversity were observed in bioassays amended with either P or NP. We suggest that climate-associated increases in phytoplankton production and concomitant shifts in diversity will influence MDV bacterial community structure by altering the availability and composition of autochthonous carbon for heterotrophic production.

10aAlgal–bacteria interactions10aclimate change10aMcMurdo Dry Valleys10aNutrient bioassay10aPrimary production1 aTeufel, Amber, G.1 aLi, Wei1 aKiss, Andor, J.1 aMorgan-Kiss, Rachael, M. uhttps://link.springer.com/article/10.1007/s00300-016-2025-803056nas a2200133 4500008004100000245014700041210006900188260003900257490001000296520251200306100001202818700002902830856006302859 2016 eng d00aInfluence of environmental drivers and interactions on the microbial community structures in permanently stratified meromictic Antarctic lakes0 aInfluence of environmental drivers and interactions on the micro aOxford, OHbMiami Universityc20160 vPh.D.3 a

The microbial loop plays important roles in the cycling of energy, carbon and elements in aquatic ecosystems. Viruses, bacteria, Archaea and microbial eukaryotes are key players in global carbon cycle and biogeochemical cycles. Investigating microbial diversity and community structure is crucial first step for understanding the ecological functioning in aquatic environment. Meromictic lakes are bodies of water and exhibit permanent stratification of major physical and chemical environmental factors. Microbial consortia residing in permanently stratified lakes exhibit relatively constant spatial stratification throughout the water column and are adapted to vastly different habitats within the same water. Pristine perennially-ice-covered lakes (Lake Bonney, Lake Fryxell and Lake Vanda) are meromictic lakes located in the McMurdo Dry Valleys (MDV) of Southern Victoria Land, Antarctica. The lakes have isolated water bodies and extremely stable strata that vary physically, chemically, and biologically within and between the water columns. The unique characteristics support microbially dominated food webs in these lakes.

In the research presented here, we gathered new understanding of how environmental drivers influence microbial community structure in these aquatic ecosystems. We explored the lake microbial ecology from three major approaches: 1). Assess trophic activities in the natural environment and identify potential environmental drivers impacting heterotrophic (β Glucosaminidase) and autotrophic (Ribulose 1,5 bisphosphate carboxylase) enzyme activities; 2). Resolve the protist community composition (i.e. autotrophic, heterotrophic and mixotrophic groups) based on high throughput sequencing and bioinformatics. Identify how the community structures correlate with specific environmental and biological factors; 3). Reveal the diversity of potential microbial interactions between the microorganisms in the MDV lakes at individual cell level, and investigate how the interactions vary between organisms with different nutritional strategies.

Studies of polar microbial communities on the cusp of environmental change will be important for predicting how microbial communities in low latitude aquatic systems will respond. This study expands the understanding of how environmental drivers interact with microbial communities in the Antarctica lakes, and provide new information to predict how the community structure will alter as response to climate changes.

1 aLi, Wei1 aMorgan-Kiss, Rachael, M. uhttp://rave.ohiolink.edu/etdc/view?acc_num=miami146975731600943nas a2200253 4500008004100000022001400041245008700055210006900142260001600211300001400227490000700241100002200248700002100270700002600291700002500317700001200342700002900354700002100383700002100404700002800425700002700453700002200480856018700502 2016 eng d a0006-356800aResponses of Antarctic Marine and Freshwater Ecosystems to Changing Ice Conditions0 aResponses of Antarctic Marine and Freshwater Ecosystems to Chang cJan-10-2016 a864 - 8790 v661 aObryk, Maciek, K.1 aDoran, Peter, T.1 aFriedlaender, Ari, S.1 aGooseff, Michael, N.1 aLi, Wei1 aMorgan-Kiss, Rachael, M.1 aPriscu, John, C.1 aSchofield, Oscar1 aStammerjohn, Sharon, E.1 aSteinberg, Deborah, K.1 aDucklow, Hugh, W. uhttps://academic.oup.com/bioscience/article-lookup/doi/10.1093/biosci/biw109https://academic.oup.com/bioscience/article/66/10/864/2415532/Responses-of-Antarctic-Marine-and-Freshwater04687nas a2200181 4500008004100000022001400041245015900055210006900214260001200283300001600295490000700311520405500318100001204373700001804385700002904403700001804432856005504450 2016 eng d a0099-224000aUltrastructural and Single-Cell-Level Characterization Reveals Metabolic Versatility in a Microbial Eukaryote Community from an Ice-Covered Antarctic Lake0 aUltrastructural and SingleCellLevel Characterization Reveals Met c06/2016 a3659 - 36700 v823 a

The McMurdo Dry Valleys (MCM) of southern Victoria Land, Antarctica, harbor numerous ice-covered bodies of water that provide year-round liquid water oases for isolated food webs dominated by the microbial loop. Single-cell microbial eukaryotes (protists) occupy major trophic positions within this truncated food web, ranging from primary producers (e.g., chlorophytes, haptophytes, and cryptophytes) to tertiary predators (e.g., ciliates, dinoflagellates, and choanoflagellates). To advance the understanding of MCM protist ecology and the roles of MCM protists in nutrient and energy cycling, we investigated potential metabolic strategies and microbial interactions of key MCM protists isolated from a well-described lake (Lake Bonney). Fluorescence-activated cell sorting (FACS) of enrichment cultures, combined with single amplified genome/amplicon sequencing and fluorescence microscopy, revealed that MCM protists possess diverse potential metabolic capabilities and interactions. Two metabolically distinct bacterial clades (Flavobacteria and Methylobacteriaceae) were independently associated with two key MCM lake microalgae (Isochrysis and Chlamydomonas, respectively). We also report on the discovery of two heterotrophic nanoflagellates belonging to the Stramenopila supergroup, one of which lives as a parasite ofChlamydomonas, a dominate primary producer in the shallow, nutrient-poor layers of the lake.

IMPORTANCE Single-cell eukaryotes called protists play critical roles in the cycling of organic matter in aquatic environments. In the ice-covered lakes of Antarctica, protists play key roles in the aquatic food web, providing the majority of organic carbon to the rest of the food web (photosynthetic protists) and acting as the major consumers at the top of the food web (predatory protists). In this study, we utilized a combination of techniques (microscopy, cell sorting, and genomic analysis) to describe the trophic abilities of Antarctic lake protists and their potential interactions with other microbes. Our work reveals that Antarctic lake protists rely on metabolic versatility for their energy and nutrient requirements in this unique and isolated environment.

1 aLi, Wei1 aPodar, Mircea1 aMorgan-Kiss, Rachael, M.1 aKelly, R., M. uhttp://aem.asm.org/lookup/doi/10.1128/AEM.00478-16