Characteristics, Biodiversity, and Cultivation Strategy of Low Nucleic Acid Content Bacteria

Low nucleic acid content (LNA) bacteria are ubiquitous and estimated to constitute 20%–90% of the total bacterial community in marine and freshwater environment. LNA bacteria with unique physiological characteristics, including small cell size and small genomes, can pass through 0.45-μm filtration. The researchers came up with different terminologies for low nucleic acid content bacteria based on different research backgrounds, such as: filterable bacteria, oligotrophic bacteria, and low-DNA bacteria. LNA bacteria have an extremely high level of genetic diversity and play an important role in material circulation in oligotrophic environment. However, the majority of LNA bacteria in the environment remain uncultivated. Thus, an important challenge now is to isolate more LNA bacteria from oligotrophic environments and gain insights into their unique metabolic mechanisms and ecological functions. Here, we reviewed LNA bacteria in aquatic environments, focusing on their characteristics, community structure and diversity, functions, and cultivation strategies. Exciting future prospects for LNA bacteria are also discussed.

[1]  J. Maresca,et al.  Aurantimicrobium photophilum sp. nov., a non-photosynthetic bacterium adjusting its metabolism to the diurnal light cycle and reclassification of Cryobacterium mesophilum as Terrimesophilobacter mesophilus gen. nov., comb. nov. , 2021, International journal of systematic and evolutionary microbiology.

[2]  L. Khandeparker,et al.  Ecological relevance of high and low nucleic acid content bacteria in a monsoon influenced tropical estuary: Implications on the β-Glucosidase activity , 2021 .

[3]  M. Hahn,et al.  Aquiluna borgnonia gen. nov., sp. nov., a member of a Microbacteriaceae lineage of freshwater bacteria with small genome sizes. , 2021, International journal of systematic and evolutionary microbiology.

[4]  D. Z. Sousa,et al.  Innovations to culturing the uncultured microbial majority , 2020, Nature Reviews Microbiology.

[5]  R. Nakai Size Matters: Ultra-small and Filterable Microorganisms in the Environment , 2020, Microbes and environments.

[6]  N. Suzina,et al.  Ultramicrobacteria , 2020, eLS.

[7]  M. Hahn,et al.  Rhodoluna limnophila sp. nov., a bacterium with 1.4 Mbp genome size isolated from freshwater habitats located in Salzburg, Austria. , 2019, International journal of systematic and evolutionary microbiology.

[8]  Yingying Wang,et al.  Passage and community changes of filterable bacteria during microfiltration of a surface water supply. , 2019, Environment international.

[9]  F. Gonçalves,et al.  Flow cytometry analysis of low/high DNA content (LNA/HNA) bacteria as bioindicator of water quality evaluation , 2019, Ecological Indicators.

[10]  Tong Zhang,et al.  New insights into antibiotic resistome in drinking water and management perspectives: A metagenomic based study of small-sized microbes. , 2019, Water research.

[11]  Yingying Wang,et al.  Impact of planktonic low nucleic acid-content bacteria to bacterial community structure and associated ecological functions in a shallow lake. , 2019, The Science of the total environment.

[12]  M. Bartlam,et al.  Structural and Functional Changes of Groundwater Bacterial Community During Temperature and pH Disturbances , 2019, Microbial Ecology.

[13]  Guijuan Zhang,et al.  Occurrence and Fate of Ultramicrobacteria in a Full-Scale Drinking Water Treatment Plant , 2018, Front. Microbiol..

[14]  David L. Jones,et al.  Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function , 2018, Front. Microbiol..

[15]  E. Lang,et al.  Polynucleobacter hirudinilacicola sp. nov. and Polynucleobacter campilacus sp. nov., both isolated from freshwater systems. , 2018, International journal of systematic and evolutionary microbiology.

[16]  Jang-Cheon Cho,et al.  Culturing the ubiquitous freshwater actinobacterial acI lineage by supplying a biochemical ‘helper’ catalase , 2018, The ISME Journal.

[17]  H. Bürgmann,et al.  Phylogenetic clustering of small low nucleic acid-content bacteria across diverse freshwater ecosystems , 2018, The ISME Journal.

[18]  Y. Shirai,et al.  Shift of low to high nucleic acid bacteria as a potential bioindicator for the screening of anthropogenic effects in a receiving river due to palm oil mill effluent final discharge , 2018 .

[19]  N. Kyrpides,et al.  Reclassification of a Polynucleobacter cosmopolitanus strain isolated from tropical Lake Victoria as Polynucleobacter victoriensis sp. nov. , 2017, International journal of systematic and evolutionary microbiology.

[20]  Yingying Wang,et al.  Geographic distribution pattern of low and high nucleic acid content bacteria on a river-catchment scale , 2017 .

[21]  B. Faircloth,et al.  Cultivation and genomics of the first freshwater SAR11 (LD12) isolate , 2017, The ISME Journal.

[22]  S. Giovannoni SAR11 Bacteria: The Most Abundant Plankton in the Oceans. , 2017, Annual review of marine science.

[23]  A. Fujiyama,et al.  Complete Genome Sequence of Aurantimicrobium minutum Type Strain KNCT, a Planktonic Ultramicrobacterium Isolated from River Water , 2016, Genome Announcements.

[24]  L. Alonso-Sáez,et al.  Experimental Warming Decreases the Average Size and Nucleic Acid Content of Marine Bacterial Communities , 2016, Front. Microbiol..

[25]  M. Bartlam,et al.  Spatio-Temporal Variations of High and Low Nucleic Acid Content Bacteria in an Exorheic River , 2016, PloS one.

[26]  Douglas G. Scofield,et al.  Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria , 2016, The ISME Journal.

[27]  M. Bartlam,et al.  Genome Sequence of a Typical Ultramicrobacterium, Curvibacter sp. Strain PAE-UM, Capable of Phthalate Ester Degradation , 2016, Genome Announcements.

[28]  T. Baba,et al.  Aurantimicrobium minutum gen. nov., sp. nov., a novel ultramicrobacterium of the family Microbacteriaceae, isolated from river water. , 2015, International journal of systematic and evolutionary microbiology.

[29]  James C. Stegen,et al.  The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle , 2015, Front. Microbiol..

[30]  H. Ducklow,et al.  More, smaller bacteria in response to ocean's warming? , 2015, Proceedings of the Royal Society B: Biological Sciences.

[31]  S. Tringe,et al.  Diverse uncultivated ultra-small bacterial cells in groundwater , 2015, Nature Communications.

[32]  A. Moya,et al.  Evolution of small prokaryotic genomes , 2015, Front. Microbiol..

[33]  S. Yooseph,et al.  Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle , 2014, Proceedings of the National Academy of Sciences.

[34]  W. Doolittle,et al.  Rhodoluna lacicola gen. nov., sp. nov., a planktonic freshwater bacterium with stream-lined genome , 2014, International journal of systematic and evolutionary microbiology.

[35]  Uwe Schröder,et al.  Cytometric fingerprints: evaluation of new tools for analyzing microbial community dynamics , 2014, Front. Microbiol..

[36]  A. Lopez-Urrutia,et al.  Automated clustering of heterotrophic bacterioplankton in flow cytometry data , 2014 .

[37]  Brian C. Thomas,et al.  Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla , 2013, mBio.

[38]  F. Rodríguez-Valera,et al.  Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria , 2013, Scientific Reports.

[39]  Natalia N. Ivanova,et al.  Insights into the phylogeny and coding potential of microbial dark matter , 2013, Nature.

[40]  P. Pevzner,et al.  Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum , 2013, Proceedings of the National Academy of Sciences.

[41]  X. Morán,et al.  Dynamics of heterotrophic bacteria in temperate coastal waters: similar net growth but different controls in low and high nucleic acid cells , 2012 .

[42]  A. Boronin,et al.  Ultramicrobacteria: Formation of the concept and contribution of ultramicrobacteria to biology , 2012, Microbiology.

[43]  M. Moran,et al.  Community analysis of high- and low-nucleic acid-containing bacteria in NW Mediterranean coastal waters using 16S rDNA pyrosequencing. , 2012, Environmental microbiology.

[44]  Ruben E. Valas,et al.  Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage , 2011, The ISME Journal.

[45]  Frank Oliver Glöckner,et al.  Phylogenetic characterisation of picoplanktonic populations with high and low nucleic acid content in the North Atlantic Ocean. , 2011, Systematic and applied microbiology.

[46]  Daniel Patrick Smith,et al.  One Carbon Metabolism in SAR11 Pelagic Marine Bacteria , 2011, PloS one.

[47]  A. Boronin,et al.  Novel ultramicrobacteria, strains NF4 and NF5, of the genus Chryseobacterium: Facultative epibionts of Bacillus subtilis , 2011, Microbiology.

[48]  J. Pernthaler,et al.  Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12) , 2011, The ISME Journal.

[49]  M. Pujo-Pay,et al.  Vertical and longitudinal gradients in HNA-LNA cell abundances and cytometric characteristics in the Mediterranean Sea , 2011 .

[50]  H. Liesegang,et al.  Comparative genome analysis and genome-guided physiological analysis of Roseobacter litoralis , 2011, BMC Genomics.

[51]  T. Egli How to live at very low substrate concentration. , 2010, Water research.

[52]  Willy Verstraete,et al.  Past, present and future applications of flow cytometry in aquatic microbiology. , 2010, Trends in biotechnology.

[53]  J. Gonzalez,et al.  Characterization of two aerobic ultramicrobacteria isolated from urban soil and a description of Oxalicibacterium solurbis sp. nov. , 2010, FEMS microbiology letters.

[54]  Marc Weber,et al.  Phylogenetic diversity and metagenomics of candidate division OP3. , 2010, Environmental microbiology.

[55]  S. Lute,et al.  Use of Hydrogenophaga pseudoflava Penetration To Quantitatively Assess the Impact of Filtration Parameters for 0.2-Micrometer-Pore-Size Filters , 2009, Applied and Environmental Microbiology.

[56]  A. Boronin,et al.  A cytological characterization of the parasitic action of ultramicrobacteria NF1 and NF3 of the genus Kaistia on chemoorganotrophic and phototrophic bacteria. , 2009, FEMS microbiology ecology.

[57]  T. Egli,et al.  Isolation and characterization of low nucleic acid (LNA)-content bacteria , 2009, The ISME Journal.

[58]  C. Nozais,et al.  Variations of the abundance and nucleic acid content of heterotrophic bacteria in Beaufort Shelf waters during winter and spring , 2008 .

[59]  Yingying Wang,et al.  The impact of industrial-scale cartridge filtration on the native microbial communities from groundwater. , 2008, Water research.

[60]  S. Giovannoni,et al.  SAR11 marine bacteria require exogenous reduced sulphur for growth , 2008, Nature.

[61]  Yingying Wang,et al.  Quantification of the filterability of freshwater bacteria through 0.45, 0.22, and 0.1 microm pore size filters and shape-dependent enrichment of filterable bacterial communities. , 2007, Environmental science & technology.

[62]  J. Gasol,et al.  A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems. , 2007, Environmental microbiology.

[63]  T. Egli,et al.  Growth of Vibrio cholerae O1 Ogawa Eltor in freshwater. , 2007, Microbiology.

[64]  C. Rezende,et al.  Distribution of HNA and LNA bacterial groups in the Southwest Atlantic Ocean , 2007 .

[65]  R. Amann,et al.  SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic Meridional Transect , 2006 .

[66]  C. Pedrós-Alió,et al.  Leeuwenhoekiella blandensis sp. nov., a genome-sequenced marine member of the family Flavobacteriaceae. , 2006, International journal of systematic and evolutionary microbiology.

[67]  E. Sherr,et al.  Variation in cell-specific rates of leucine and thymidine incorporation by marine bacteria with high and with low nucleic acid content off the Oregon coast , 2006 .

[68]  Glen A. Tarran,et al.  Bacterioplankton of low and high DNA content in the suboxic waters of the Arabian Sea and the Gulf of Oman : abundance and amino acid uptake , 2006 .

[69]  E. Sherr,et al.  Activity and Phylogenetic Diversity of Bacterial Cells with High and Low Nucleic Acid Content and Electron Transport System Activity in an Upwelling Ecosystem , 2005, Applied and Environmental Microbiology.

[70]  V. Miteva,et al.  Detection and Isolation of Ultrasmall Microorganisms from a 120,000-Year-Old Greenland Glacier Ice Core , 2005, Applied and Environmental Microbiology.

[71]  Chulgoo Kim,et al.  Vertical and Seasonal Variations of Bacterioplankton Subgroups with Different Nucleic Acid Contents: Possible Regulation by Phosphorus , 2005, Applied and Environmental Microbiology.

[72]  M. Noordewier,et al.  Genome Streamlining in a Cosmopolitan Oceanic Bacterium , 2005, Science.

[73]  Matthew R. First,et al.  Growth and grazing rates of bacteria groups with different apparent DNA content in the Gulf of Mexico , 2004 .

[74]  E. Casamayor,et al.  Activity and diversity of bacterial cells with high and low nucleic acid content , 2003 .

[75]  R. Cavicchioli,et al.  Life under Nutrient Limitation in Oligotrophic Marine Environments: An Eco/Physiological Perspective of Sphingopyxis alaskensis (formerly Sphingomonas alaskensis) , 2003, Microbial Ecology.

[76]  M. Höfle,et al.  Isolation of Novel Ultramicrobacteria Classified as Actinobacteria from Five Freshwater Habitats in Europe and Asia , 2003, Applied and Environmental Microbiology.

[77]  R. Amann,et al.  Mesoscale distribution of dominant bacterioplankton groups in the northern North Sea in early summer , 2002 .

[78]  S. Giovannoni,et al.  High-Throughput Methods for Culturing Microorganisms in Very-Low-Nutrient Media Yield Diverse New Marine Isolates , 2002, Applied and Environmental Microbiology.

[79]  P. Servais,et al.  Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry , 2002 .

[80]  K. Lewis,et al.  Isolating "Uncultivable" Microorganisms in Pure Culture in a Simulated Natural Environment , 2002, Science.

[81]  R. Amann,et al.  Comparison of Cellular and Biomass Specific Activities of Dominant Bacterioplankton Groups in Stratified Waters of the Celtic Sea , 2001, Applied and Environmental Microbiology.

[82]  Philippe Lebaron,et al.  Does the High Nucleic Acid Content of Individual Bacterial Cells Allow Us To Discriminate between Active Cells and Inactive Cells in Aquatic Systems? , 2001, Applied and Environmental Microbiology.

[83]  R. Cavicchioli,et al.  Specific Growth Rate Plays a Critical Role in Hydrogen Peroxide Resistance of the Marine Oligotrophic UltramicrobacteriumSphingomonas alaskensis Strain RB2256 , 2001, Applied and Environmental Microbiology.

[84]  Josep M. Gasol,et al.  Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities , 2000 .

[85]  M. Cottrell,et al.  Natural Assemblages of Marine Proteobacteria and Members of the Cytophaga-Flavobacter Cluster Consuming Low- and High-Molecular-Weight Dissolved Organic Matter , 2000, Applied and Environmental Microbiology.

[86]  J. Fuhrman,et al.  Significance of Size and Nucleic Acid Content Heterogeneity as Measured by Flow Cytometry in Natural Planktonic Bacteria , 1999, Applied and Environmental Microbiology.

[87]  G. Tarran,et al.  Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S , 1998 .

[88]  J. Gottschal,et al.  Isolation and characterisation of the marine ultramicrobacterium Sphingomonas sp. strain RB2256 , 1997 .

[89]  M. Sieracki,et al.  CELLULAR DNA CONTENT OF MARINE PHYTOPLANKTON USING TWO NEW FLUOROCHROMES: TAXONOMIC AND ECOLOGICAL IMPLICATIONS 1 , 1997 .

[90]  D. Vaulot,et al.  Enumeration and Cell Cycle Analysis of Natural Populations of Marine Picoplankton by Flow Cytometry Using the Nucleic Acid Stain SYBR Green I , 1997, Applied and environmental microbiology.

[91]  S. Kjelleberg,et al.  Responses to Stress and Nutrient Availability by the Marine Ultramicrobacterium Sphingomonas sp. Strain RB2256 , 1996, Applied and environmental microbiology.

[92]  William K. W. Li,et al.  DNA distributions in planktonic bacteria stained with TOTO or TO‐PRO , 1995 .

[93]  Egbert J. de Vries,et al.  Isolation of Typical Marine Bacteria by Dilution Culture: Growth, Maintenance, and Characteristics of Isolates under Laboratory Conditions , 1993, Applied and environmental microbiology.

[94]  D. Button,et al.  Viability and Isolation of Marine Bacteria by Dilution Culture: Theory, Procedures, and Initial Results , 1993, Applied and environmental microbiology.

[95]  Mitsuru Nomura,et al.  Layered coding for ATM based video distribution systems , 1991, Signal Process. Image Commun..

[96]  R. Y. Morita,et al.  Bioavailability of energy and its relationship to growth and starvation survival in nature , 1988 .

[97]  R. Colwell,et al.  Filterable marine bacteria found in the deep sea: Distribution, taxonomy, and response to starvation , 1981, Microbial Ecology.

[98]  R. Y. Morita,et al.  Microcultural Study of Bacterial Size Changes and Microcolony and Ultramicrocolony Formation by Heterotrophic Bacteria in Seawater , 1981, Applied and environmental microbiology.

[99]  E. Lang,et al.  Polynucleobacter paneuropaeus sp. nov., characterized by six strains isolated from freshwater lakes located along a 3000 km north-south cross-section across Europe. , 2019, International journal of systematic and evolutionary microbiology.

[100]  ISOLATION AND CHARACTERISATION , 2015 .

[101]  Frederik Hammes,et al.  Kinetics of membrane damage to high (HNA) and low (LNA) nucleic acid bacterial clusters in drinking water by ozone, chlorine, chlorine dioxide, monochloramine, ferrate(VI), and permanganate. , 2011, Water research.

[102]  E. Stackebrandt,et al.  Polynucleobacter cosmopolitanus sp. nov., free-living planktonic bacteria inhabiting freshwater lakes and rivers. , 2010, International journal of systematic and evolutionary microbiology.

[103]  V. Miteva,et al.  Novel ultramicrobacterial isolates from a deep Greenland ice core represent a proposed new species, Chryseobacterium greenlandense sp. nov. , 2009, Extremophiles.