16S ribosomal RNA

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Molecular structure of the 30S Subunit from Thermus thermophilus. Proteins are shown in blue and the single RNA strand in a pale orange-brown colour. 010 small subunit-1FKA.gif
Molecular structure of the 30S Subunit from Thermus thermophilus . Proteins are shown in blue and the single RNA strand in a pale orange-brown colour.

16S ribosomal RNA (or 16S rRNA) is the RNA component of the 30S subunit of a prokaryotic ribosome (SSU rRNA). It binds to the Shine-Dalgarno sequence and provides most of the SSU structure.

Contents

The genes coding for it are referred to as 16S rRNA genes and are used in reconstructing phylogenies, due to the slow rates of evolution of this region of the gene. [2] Carl Woese and George E. Fox were two of the people who pioneered the use of 16S rRNA in phylogenetics in 1977. [3] Multiple sequences of the 16S rRNA gene can exist within a single bacterium. [4]

Functions

Structure

SSU Ribosomal RNA, bacteria and archaea. From Woese 1987. 16S.svg
SSU Ribosomal RNA, bacteria and archaea. From Woese 1987.

Universal primers

The 16S rRNA gene is used for phylogenetic studies [7] as it is highly conserved between different species of bacteria and archaea. [8] Carl Woese pioneered this use of 16S rRNA in 1977. [2] It is suggested that 16S rRNA gene can be used as a reliable molecular clock because 16S rRNA sequences from distantly related bacterial lineages are shown to have similar functionalities. [9] Some thermophilic archaea (e.g. order Thermoproteales) contain 16S rRNA gene introns that are located in highly conserved regions and can impact the annealing of "universal" primers. [10] Mitochondrial and chloroplastic rRNA are also amplified. [11]

The most common primer pair was devised by Weisburg et al. (1991) [7] and is currently referred to as 27F and 1492R; however, for some applications shorter amplicons may be necessary, for example for 454 sequencing with titanium chemistry the primer pair 27F-534R covering V1 to V3. [12] Often 8F is used rather than 27F. The two primers are almost identical, but 27F has an M instead of a C. AGAGTTTGATCMTGGCTCAG compared with 8F. [13]

Primer nameSequence (5′–3′)Ref.
8FAGA GTT TGA TCC TGG CTC AG [14] [15]
27FAGA GTT TGA TCM TGG CTC AG [13]
336RACT GCT GCS YCC CGT AGG AGT CT [16]
337FGAC TCC TAC GGG AGG CWG CAG [17]
518RGTA TTA CCG CGG CTG CTG G
533FGTG CCA GCM GCC GCG GTA A
785FGGA TTA GAT ACC CTG GTA
806RGGA CTA CVS GGG TAT CTA AT [18] [19]
907RCCG TCA ATT CCT TTR AGT TT
928FTAA AAC TYA AAK GAA TTG ACG GG [16]
1100FYAA CGA GCG CAA CCC
1100RGGG TTG CGC TCG TTG
U1492RGGT TAC CTT GTT ACG ACT T [14] [15]
1492RCGG TTA CCT TGT TAC GAC TT [20]

PCR and NGS applications

In addition to highly conserved primer binding sites, 16S rRNA gene sequences contain hypervariable regions that can provide species-specific signature sequences useful for identification of bacteria. [21] [22] As a result, 16S rRNA gene sequencing has become prevalent in medical microbiology as a rapid and cheap alternative to phenotypic methods of bacterial identification. [23] Although it was originally used to identify bacteria, 16S sequencing was subsequently found to be capable of reclassifying bacteria into completely new species, [24] or even genera. [7] [25] It has also been used to describe new species that have never been successfully cultured. [26] [27] With third-generation sequencing coming to many labs, simultaneous identification of thousands of 16S rRNA sequences is possible within hours, allowing metagenomic studies, for example of gut flora. [28] In samples collected from patients with confirmed infections, 16S rRNA next-generation sequencing (NGS) demonstrated enhanced detection in 40% of cases compared to traditional culture methods; moreover, pre-sampling antibiotic consumption did not significantly affect the sensitivity of 16S NGS. [29]

Hypervariable regions

The bacterial 16S gene contains nine hypervariable regions (V1–V9), ranging from about 30 to 100 base pairs long, that are involved in the secondary structure of the small ribosomal subunit. [30] The degree of conservation varies widely between hypervariable regions, with more conserved regions correlating to higher-level taxonomy and less conserved regions to lower levels, such as genus and species. [31] While the entire 16S sequence allows for comparison of all hypervariable regions, at approximately 1,500 base pairs long it can be prohibitively expensive for studies seeking to identify or characterize diverse bacterial communities. [31] These studies commonly utilize the Illumina platform, which produces reads at rates 50-fold and 12,000-fold less expensive than 454 pyrosequencing and Sanger sequencing, respectively. [32] While cheaper and allowing for deeper community coverage, Illumina sequencing only produces reads 75–250 base pairs long (up to 300 base pairs with Illumina MiSeq), and has no established protocol for reliably assembling the full gene in community samples. [33] Full hypervariable regions can be assembled from a single Illumina run, however, making them ideal targets for the platform. [33]

While 16S hypervariable regions can vary dramatically between bacteria, the 16S gene as a whole maintains greater length homogeneity than its eukaryotic counterpart (18S ribosomal RNA), which can make alignments easier. [34] Additionally, the 16S gene contains highly conserved sequences between hypervariable regions, enabling the design of universal primers that can reliably produce the same sections of the 16S sequence across different taxa. [35] Although no hypervariable region can accurately classify all bacteria from domain to species, some can reliably predict specific taxonomic levels. [31] Many community studies select semi-conserved hypervariable regions like the V4 for this reason, as it can provide resolution at the phylum level as accurately as the full 16S gene. [31] While lesser-conserved regions struggle to classify new species when higher order taxonomy is unknown, they are often used to detect the presence of specific pathogens. In one study by Chakravorty et al. in 2007, the authors characterized the V1–V8 regions of a variety of pathogens in order to determine which hypervariable regions would be most useful to include for disease-specific and broad assays. [36] Amongst other findings, they noted that the V3 region was best at identifying the genus for all pathogens tested, and that V6 was the most accurate at differentiating species between all CDC-watched pathogens tested, including anthrax. [36]

While 16S hypervariable region analysis is a powerful tool for bacterial taxonomic studies, it struggles to differentiate between closely related species. [35] In the families Enterobacteriaceae , Clostridiaceae , and Peptostreptococcaceae , species can share up to 99% sequence similarity across the full 16S gene. [37] As a result, the V4 sequences can differ by only a few nucleotides, leaving reference databases unable to reliably classify these bacteria at lower taxonomic levels. [37] By limiting 16S analysis to select hypervariable regions, these studies can fail to observe differences in closely related taxa and group them into single taxonomic units, therefore underestimating the total diversity of the sample. [35] Furthermore, bacterial genomes can house multiple 16S genes, with the V1, V2, and V6 regions containing the greatest intraspecies diversity. [8] While not the most precise method of classifying bacterial species, analysis of the hypervariable regions remains one of the most useful tools available to bacterial community studies. [37]

Promiscuity of 16S rRNA genes

Under the assumption that evolution is driven by vertical transmission, 16S rRNA genes have long been believed to be species-specific, and infallible as genetic markers inferring phylogenetic relationships among prokaryotes. However, a growing number of observations suggest the occurrence of horizontal transfer of these genes. In addition to observations of natural occurrence, transferability of these genes is supported experimentally using a specialized Escherichia coli genetic system. Using a null mutant of E. coli as host, growth of the mutant strain was shown to be complemented by foreign 16S rRNA genes that were phylogenetically distinct from E. coli at the phylum level. [38] [39] Such functional compatibility was also seen in Thermus thermophilus . [40] Furthermore, in T. thermophilus, both complete and partial gene transfer was observed. Partial transfer resulted in spontaneous generation of apparently random chimera between host and foreign bacterial genes. Thus, 16S rRNA genes may have evolved through multiple mechanisms, including vertical inheritance and horizontal gene transfer; the frequency of the latter may be much higher than previously thought. [41]

16S ribosomal databases

The 16S rRNA gene is used as the standard for classification and identification of microbes, because it is present in most microbes and shows proper changes. [42] Type strains of 16S rRNA gene sequences for most bacteria and archaea are available on public databases, such as NCBI. However, the quality of the sequences found on these databases is often not validated. Therefore, secondary databases that collect only 16S rRNA sequences are widely used.

MIMt

MIMt is a compact non-redundant 16S database for a rapid metagenomic samples identification. It is composed of 48.749 full 16S sequences belonging to 24,626 well classified bacteria and archaea species. All sequences were obtained from complete genomes deposited in NCBI and for each of the sequences full taxonomic hierarchy is provided. It contains no redundancy, so only one representative for each species was considered avoiding same sequences from differente strains, isolates or patovars resulting in a very fast tool for microorganisms identification, compatible with any classification software (QIIME, Mothur, DADA, etc). [43]

EzBioCloud

EzBioCloud database, formerly known as EzTaxon, consists of a complete hierarchical taxonomic system containing 62,988 bacteria and archaea species/phylotypes which includes 15,290 valid published names as of September 2018. Based on the phylogenetic relationship such as maximum-likelihood and OrthoANI, all species/subspecies are represented by at least one 16S rRNA gene sequence. The EzBioCloud database is systematically curated and updated regularly which also includes novel candidate species. Moreover, the website provides bioinformatics tools such as ANI calculator, ContEst16S and 16S rRNA DB for QIIME and Mothur pipeline. [44] ^^

Ribosomal Database Project

The Ribosomal Database Project (RDP) is a curated database that offers ribosome data along with related programs and services. The offerings include phylogenetically ordered alignments of ribosomal RNA (rRNA) sequences, derived phylogenetic trees, rRNA secondary structure diagrams and various software packages for handling, analyzing and displaying alignments and trees. The data are available via ftp and electronic mail. Certain analytic services are also provided by the electronic mail server. [45] Due to its large size the RDP database is often used as the basis for bioinformatic tool development and creating manually curated databases. [46]

SILVA

SILVA provides comprehensive, quality checked and regularly updated datasets of aligned small (16S/18S, SSU) and large subunit (23S/28S, LSU) ribosomal RNA (rRNA) sequences for all three domains of life as well as a suite of search, primer-design and alignment tools (Bacteria, Archaea and Eukarya). [47]

GreenGenes

GreenGenes is a quality controlled, comprehensive 16S rRNA gene reference database and taxonomy based on a de novo phylogeny that provides standard operational taxonomic unit sets. Beware that it utilizes taxonomic terms proposed from phylogenetic methods applied years ago between 2012 and 2013. Since then, a variety of novel phylogenetic methods have been proposed for Archaea and Bacteria. [48] [49]

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<span class="mw-page-title-main">Carl Woese</span> American microbiologist (1928–2012)

Carl Richard Woese was an American microbiologist and biophysicist. Woese is famous for defining the Archaea in 1977 through a pioneering phylogenetic taxonomy of 16S ribosomal RNA, a technique that has revolutionized microbiology. He also originated the RNA world hypothesis in 1967, although not by that name. Woese held the Stanley O. Ikenberry Chair and was professor of microbiology at the University of Illinois Urbana–Champaign.

<span class="mw-page-title-main">Domain (biology)</span> Taxonomic rank

In biological taxonomy, a domain, also dominion, superkingdom, realm, or empire, is the highest taxonomic rank of all organisms taken together. It was introduced in the three-domain system of taxonomy devised by Carl Woese, Otto Kandler and Mark Wheelis in 1990.

<span class="mw-page-title-main">Three-domain system</span> Hypothesis for classification of life

The three-domain system is a taxonomic classification system that groups all cellular life into three domains, namely Archaea, Bacteria and Eukarya, introduced by Carl Woese, Otto Kandler and Mark Wheelis in 1990. The key difference from earlier classifications such as the two-empire system and the five-kingdom classification is the splitting of Archaea from Bacteria as completely different organisms. It has been challenged by the two-domain system that divides organisms into Bacteria and Archaea only, as Eukaryotes are considered a clade of Archaea.

<span class="mw-page-title-main">Nanoarchaeota</span> Phylum of archaea

Nanoarchaeota is a proposed phylum in the domain Archaea that currently has only one representative, Nanoarchaeum equitans, which was discovered in a submarine hydrothermal vent and first described in 2002.

<span class="mw-page-title-main">Thermoproteota</span> Phylum of archaea

The Thermoproteota are prokaryotes that have been classified as a phylum of the domain Archaea. Initially, the Thermoproteota were thought to be sulfur-dependent extremophiles but recent studies have identified characteristic Thermoproteota environmental rRNA indicating the organisms may be the most abundant archaea in the marine environment. Originally, they were separated from the other archaea based on rRNA sequences; other physiological features, such as lack of histones, have supported this division, although some crenarchaea were found to have histones. Until 2005 all cultured Thermoproteota had been thermophilic or hyperthermophilic organisms, some of which have the ability to grow at up to 113 °C. These organisms stain Gram negative and are morphologically diverse, having rod, cocci, filamentous and oddly-shaped cells. Recent evidence shows that some members of the Thermoproteota are methanogens.

<span class="mw-page-title-main">Korarchaeota</span> Proposed phylum within the Archaea

The Korarchaeota is a proposed phylum within the Archaea. The name is derived from the Greek noun koros or kore, meaning young man or young woman, and the Greek adjective archaios which means ancient. They are also known as Xenarchaeota. The name is equivalent to Candidatus Korarchaeota, and they go by the name Xenarchaeota or Xenarchaea as well.

The ribosomal DNA consists of a group of ribosomal RNA encoding genes and related regulatory elements, and is widespread in similar configuration in all domains of life. The ribosomal DNA encodes the non-coding ribosomal RNA, integral structural elements in the assembly of ribosomes, its importance making it the most abundant section of RNA found in cells of eukaryotes. Additionally, these segments includes regulatory sections, such as a promotor specific to the RNA polymerase I, as well as both transcribed and non-transcribed spacer segments.

Internal transcribed spacer (ITS) is the spacer DNA situated between the small-subunit ribosomal RNA (rRNA) and large-subunit rRNA genes in the chromosome or the corresponding transcribed region in the polycistronic rRNA precursor transcript.

<span class="mw-page-title-main">George E. Fox</span> American astrobiologist

George Edward Fox is an astrobiologist, a Professor Emeritus and researcher at the University of Houston. He is an elected fellow of the American Academy of Microbiology, the American Association for the Advancement of Science, American Institute for Medical and Biological Engineering and the International Astrobiology Society. Fox received his B.A. degree in 1967, and completed his Ph.D. degree in 1974; both in chemical engineering at Syracuse University.

<span class="mw-page-title-main">Archaea</span> Domain of organisms

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<span class="mw-page-title-main">Bacterial phyla</span> Phyla or divisions of the domain Bacteria

Bacterial phyla constitute the major lineages of the domain Bacteria. While the exact definition of a bacterial phylum is debated, a popular definition is that a bacterial phylum is a monophyletic lineage of bacteria whose 16S rRNA genes share a pairwise sequence identity of ~75% or less with those of the members of other bacterial phyla.

<span class="mw-page-title-main">Bacterial taxonomy</span> Rank based classification of bacteria

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There are several models of the Branching order of bacterial phyla, one of these was proposed in 1987 paper by Carl Woese.

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<span class="mw-page-title-main">Eocyte hypothesis</span> Hypothesis in evolutionary biology

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