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Title: Ultrastructural and Single-Cell-Level Characterization Reveals Metabolic Versatility in a Microbial Eukaryote Community from an Ice-Covered Antarctic Lake

Journal Article · · Applied and Environmental Microbiology
 [1];  [2];  [1]
  1. Miami Univ., Oxford, OH (United States). Dept. of Microbiology
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division

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 (FlavobacteriaandMethylobacteriaceae) were independently associated with two key MCM lake microalgae (IsochrysisandChlamydomonas, 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. 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. Ultimately, our work reveals that Antarctic lake protists rely on metabolic versatility for their energy and nutrient requirements in this unique and isolated environment.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE; NSF; ORNL LDRD Director's R&D
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1319189
Journal Information:
Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 12 Vol. 82; ISSN 0099-2240
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (85)

Diversity and spatial distribution of autotrophic communities within and between ice-covered Antarctic lakes (McMurdo Dry Valleys): Autotrophic communities in Antarctic lakes journal March 2015
Protistan community structure: molecular approaches for answering ecological questions book January 1999
Paleolimnology of the McMurdo Dry Valleys, Antarctica journal January 1994
Particulate and Dissolved Organic Carbon Production by the Heterotrophic Nanoflagellate Pteridomonas danica Patterson and Fenchel journal May 1999
The distribution of microplankton in the McMurdo Dry Valley Lakes, Antarctica: response to ecosystem legacy or present-day climatic controls? journal March 2004
Review: the Antarctic Chlamydomonas raudensis: an emerging model for cold adaptation of photosynthesis journal August 2013
The Saline Lakes of the McMurdo Dry Valleys, Antarctica journal December 2008
“Missing” protists: a molecular prospective journal October 2007
On the habitability of Europa journal November 1983
Light and electron microscopical observations on Pirsonia punctigerae spec, nov., a nanoflagellate feeding on the marine centric diatom Thalassiosira punctigera journal June 1997
Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence in situ hybridization journal May 2005
Assimilation efficiency of Vibrio bacterial protein biomass by the flagellate Pteridomonas: Assessment using flow cytometric sorting journal October 2005
Highly Diverse and Seasonally Dynamic Protist Community in a Pristine Peat Bog journal January 2011
The rise of model protozoa journal April 2012
Significance of predation by protists in aquatic microbial food webs journal March 2002
Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton journal February 2001
Protists are microbes too: a perspective journal November 2008
Capturing diversity of marine heterotrophic protists: one cell at a time journal October 2010
Unveiling in situ interactions between marine protists and bacteria through single cell sequencing journal September 2011
Protist diversity in a permanently ice-covered Antarctic Lake during the polar night transition journal March 2011
In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake journal December 2012
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms journal March 2012
Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes journal October 2013
The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign journal May 2015
Marked seasonality and high spatial variability of protist communities in shallow freshwater systems journal March 2015
QIIME allows analysis of high-throughput community sequencing data journal April 2010
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics journal April 2014
Predation on prokaryotes in the water column and its ecological implications journal June 2005
Microbial interactions: from networks to models journal July 2012
Master recyclers: features and functions of bacteria associated with phytoplankton blooms journal August 2014
Microbial ecology of Antarctic aquatic systems journal October 2015
Mixotrophic cryptophytes and their predators in the Dry Valley lakes of Antarctica journal June 1999
Mixotrophy in the Antarctic Phytoflagellate, Pyramimonas Gelidicola (Chlorophyta: Prasinophyceae)1 journal July 2003
Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth journal July 2007
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample journal June 2010
Vestigial Chloroplasts in Heterotrophic Stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae) journal June 2002
Phylogenetic Position of the Parasitoid Nanoflagellate Pirsonia inferred from Nuclear-Encoded Small Subunit Ribosomal DNA and a Description of Pseudopirsonia n. gen. and Pseudopirsonia mucosa (Drebes) comb. nov. journal June 2004
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB journal November 2007
Digital MDA for enumeration of total nucleic acid contamination journal November 2010
The Photosynthetic Apparatus of Phytoplankton from a Perennially Ice-Covered Antarctic Lake: Acclimation to an Extreme Shade Environment journal March 1995
Survival mechanisms in Antarctic lakes journal July 2002
The biodiversity and ecology of Antarctic lakes: models for evolution journal May 2007
Microbial community profiling for human microbiome projects: Tools, techniques, and challenges journal April 2009
The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics : Metaproteomics of marine Antarctic journal November 2012
Interactions between specific phytoplankton and bacteria affect lake bacterial community succession: Phytoplankton affect bacterial community dynamics journal May 2013
Complex communities of small protists and unexpected occurrence of typical marine lineages in shallow freshwater systems: Protist diversity in shallow freshwater systems journal September 2014
An integrated study of photochemical function and expression of a key photochemical gene ( psbA ) in photosynthetic communities of Lake Bonney (McMurdo Dry Valleys, Antarctica) journal March 2014
Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity: HIGH SEASONAL PROTIST ABUNDANCE TURNOVER journal July 2010
Two decades of describing the unseen majority of aquatic microbial diversity: SEQUENCING AQUATIC MICROBIAL DIVERSITY journal November 2011
A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY journal February 2001
Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist: Roadmap for beta diversity journal November 2010
Marine diatom species harbour distinct bacterial communities: Marine diatom species harbour distinct bacterial communities journal March 2005
Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom journal August 2006
Differential grazing of two heterotrophic nanoflagellates on marine Synechococcus strains journal July 2009
Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom: Succession of NAG-consuming bacteria in a lake journal November 2011
Trichosarcina polymorpha Gen. et Sp. Nov. journal March 1965
The Growing Contributions of Molecular Biology and Immunology to Protistan Ecology: Molecular Signatures as Ecological Tools1 journal January 2004
The ecology of Cytophaga–Flavobacteria in aquatic environments journal February 2002
No Place Too Cold journal June 2009
Single-Cell Genomics Reveals Organismal Interactions in Uncultivated Marine Protists journal May 2011
Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean journal September 2011
Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom journal May 2012
Diversity and Expression of RubisCO Genes in a Perennially Ice-Covered Antarctic Lake during the Polar Night Transition journal April 2012
Improved Methodology for Identification of Protists and Microalgae from Plankton Samples Preserved in Lugol's Iodine Solution: Combining Microscopic Analysis with Single-Cell PCR journal April 2008
Quantitative and Qualitative   Diversity Measures Lead to Different Insights into Factors That Structure Microbial Communities journal January 2007
Flow Sorting of Marine Bacterioplankton after Fluorescence In Situ Hybridization journal October 2004
Phylogenetic and Ecological Analysis of Novel Marine Stramenopiles journal June 2004
Interactions between Diatoms and Bacteria journal August 2012
Adaptation and Acclimation of Photosynthetic Microorganisms to Permanently Cold Environments journal March 2006
Purification and properties of unicellular blue-green algae (order Chroococcales) journal June 1971
Antarctic microbial mats: A modern analog for Archean lacustrine oxygen oases journal August 2015
Studies of Marine Planktonic Diatoms: i. Cyclotella nana Hustedt, and Detonula Confervacea (Cleve) Gran. journal April 1962
A Method for Studying Protistan Diversity Using Massively Parallel Sequencing of V9 Hypervariable Regions of Small-Subunit Ribosomal RNA Genes journal July 2009
Multiple Single-Cell Genomes Provide Insight into Functions of Uncultured Deltaproteobacteria in the Human Oral Cavity journal March 2013
Phylogenetic studies on two strains of Antarctic ice algae based on morphological and molecular characteristics journal February 2006
Carbon Transformations in a Perennially Ice-Covered Antarctic Lake journal December 1999
Microbial dynamics in autotrophic and heterotrophic seawater mesocosms. II. Bacterioplankton community structure and hydrolytic enzyme activities journal November 2007
Spatio-temporal patterns of bacterioplankton production and community composition related to phytoplankton composition and protistan bacterivory in a dam reservoir journal June 2008
Mixotrophy: a widespread and important ecological strategy for planktonic and sea-ice nanoflagellates in the Ross Sea, Antarctica journal March 2009
Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring journal May 2012
Increased filtration efficiency of attached compared to free-swimming flagellates journal January 2003
Counting heterotrophic nanoplanktonic protists in cultures and aquatic communities by flow cytometry journal January 2004
Particle-associated flagellates: swimming patterns, colonization rates, and grazing on attached bacteria journal January 2004
Ecology of Heterotrophic Microflagellates. IV Quantitative Occurrence and Importance as Bacterial Consumers journal January 1982
Heterotrophic and mixotrophic nanoplankton predation on picoplankton in the Sargasso Sea and on Georges Bank journal January 2000

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