Streamlining theory

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Genomic streamlining is a theory in evolutionary biology and microbial ecology that suggests that there is a reproductive benefit to prokaryotes having a smaller genome size with less non-coding DNA and fewer non-essential genes. [1] [2] There is a lot of variation in prokaryotic genome size, with the smallest free-living cell's genome being roughly ten times smaller than the largest prokaryote. [3] Two of the free-living bacterial taxa with the smallest genomes are Prochlorococcus and Pelagibacter ubique, [4] [5] both highly abundant marine bacteria commonly found in oligotrophic regions. Similar reduced genomes have been found in uncultured marine bacteria, suggesting that genomic streamlining is a common feature of bacterioplankton. [6] This theory is typically used with reference to free-living organisms in oligotrophic environments. [1]

Contents

Overview

Comparison of genome sizes across select organisms Genome Sizes.png
Comparison of genome sizes across select organisms

Genome streamlining theory states that certain prokaryotic genomes tend to be small in size in comparison to other prokaryotes, and all eukaryotes, due to selection against the retention of non-coding DNA. [2] [1] The known advantages of small genome size include faster genome replication for cell division, fewer nutrient requirements, and easier co-regulation of multiple related genes, because gene density typically increases with decreased genome size. [2] This means that an organism with a smaller genome is likely to be more successful, or have higher fitness, than one hindered by excessive amounts of unnecessary DNA, leading to selection for smaller genome sizes. [2]

Some mechanisms that are thought to underlie genome streamlining include deletion bias and purifying selection. [1] Deletion bias is the phenomenon in bacterial genomes where the rate of DNA loss is naturally higher than the rate of DNA acquisition. [2] [7] This is a passive process that simply results from the difference in these two rates. [7] Purifying selection is the process by which extraneous genes are selected against, making organisms lacking this genetic material more successful by effectively reducing their genome size. [2] [8] Genes and non-coding DNA segments that are less crucial for an organism survival will be more likely to be lost over time. [8]

This selective pressure is stronger in large marine prokaryotic populations, because intra-species competition favours fast, efficient and inexpensive replication. [2] This is because large population sizes increase competition among members of the same species, and thus increases selective pressure and causes the reduction in genome size to occur more readily among organisms of large population sizes, like bacteria. [2] This may explain why genome streamlining seems to be particularly prevalent in prokaryotic organisms, as they tend to have larger population sizes than eukaryotes. [9]

It has also been proposed that having a smaller genome can help minimize overall cell size, which increases a prokaryotes surface-area to volume ratio. [10] A higher surface-area to volume ratio allows for more nutrient uptake proportional to their size, which allows them to outcompete other larger organisms for nutrients. [11] [10] This phenomenon has been noted particularly in nutrient depleted waters. [10]

Genomic signatures

Genomic analysis of streamlined organisms have shown that low GC content, low percentage of non-coding DNA, and a low fraction of genes encoding for cytoplasmic membrane proteins, periplasmic proteins, transcriptionally related proteins, and signal transduction pathways are all characteristic of free-living streamlined prokaryotic organisms. [6] [4] [12] Oftentimes, highly streamlined organisms are difficult to isolate by culturing in a laboratory (SAR11 being a central example). [6] [4]

Model organisms

Pelagibacter ubique (SAR11)

Pelagibacter ubique are members of the SAR11 clade, a heterotrophic marine group which are found throughout the oceans and are rather common. [4] These microbes have the smallest genome and encode the smallest number of Open Reading Frames of any known non-sessile microorganism. [4] P. ubique has complete biosynthetic pathways and all necessary enzymes for the synthesis of 20 amino acids and only lack a few cofactors despite the genome's small size. The genome size for this microorganism is achieved by lack of, "pseudogenes, introns, transposons, extrachromosomal elements, or inteins". The genome also contains fewer paralogs compared to other members of the same clade and the shortest intergenic spacers for any living cell. [4] In these organisms, unusual nutrient requirements were found due to the streamlining selection and gene loss when selection occurred for more efficient resource utilization in oceans with limited nutrients for uptake. [13] These observations indicate that some microbes may be difficult to grow in a laboratory setting because of unusual nutrient requirements. [13]

Prochlorococcus

Individual Prochlorococcus cell

Prochlorococcus is one of the dominant cyanobacteria and is a main participant in primary production in oligotrophic waters. [14] It is the smallest and most abundant photosynthetic organism recorded on Earth. [14] As a cyanobacteria, they have an incredible ability to adapt to environments with very poor nutrient availability, as they maintain their energy from light. [15] The nitrogen assimilation pathway in this organism has been significantly modified to adapt to the nutritional limitations of the organisms’ habitats. [15] These adaptations led to the removal of key enzymes from the genome, such as nitrate reductase, nitrite reductase, and often urease. [15] Unlike some cyanobacterial counterparts, Prochlorococcus is not able to fix atmospheric nitrogen (N2). [16] The only nitrogen sources found to be used by this species are ammonia, which is incorporated into glutamate via the enzyme glutamine synthetase and uses less energy compared to nitrate usage, and in certain species, urea. [16] Moreover, metabolic regulation systems of Prochlorococcus were found to be greatly simplified. [15]

Nitrogen-fixing marine cyanobacteria (UCYN-A)

Cyanobacteria blooms on a lake Cyanobacteria Aggregation2.jpg
Cyanobacteria blooms on a lake

Nitrogen-fixing marine cyanobacteria are known to support oxygen production in oceans by fixing inorganic nitrogen using the enzyme nitrogenase. [17] A special subset of these bacteria, UCYN-A, was found to lack the photosystem II complex usually used in photosynthesis and that it lacks a number of major metabolic pathways but is still capable of using the electron transport chain to generate energy from a light source. [17] Furthermore, anabolic enzymes needed for creating amino acids such as valine, leucine and isoleucine are missing, as well as some which lead to phenylalanine, tyrosine and tryptophan biosynthesis.

This organism seems to be an obligate photoheterotroph that uses carbon substrates for energy production and some biosynthetic materials for biosynthesis. It was discovered that UCYN-A developed a reduced genome of only 1.44 Megabases that is smaller but similar in structure to that of chloroplasts. [17] In comparison with related species such as Crocosphaera watsonii and Cyanothece sp., which employ genomes which range in length from 5.46 to 6.24 megabases, the UCYN-A genome is much smaller. The compacted genome is a single, circular chromosome with “1,214 identified protein-coding regions”. [17] The genome of UCYN-A is also highly conserved ( >97% nucleotide identity) across ocean waters, which is atypical of ocean microbes. The lack of UCYN-A genome diversity, presence of nitrogenase and hydrogenase enzymes for the TCA cycle, reduced genome size and coding efficiency of the DNA suggest that this microorganism may have symbiotic lifestyle and live in close association with a host. However, the true lifestyle of this microbe remains unknown. [17]

Alternative cases of small genomes

Bacterial symbionts, commensals, parasites, and pathogens

Bacterial symbionts, commensals, parasites, and pathogens often have even smaller genomes and fewer genes than free-living organisms, and non-pathogenic bacteria. [1] They reduce their "core" metabolic repertoire, making them more dependent on their host and environment. [1] Their genome reduction occurs by different evolutionary mechanisms than those of streamlined free-living organisms. [18] Pathogenic organisms are thought to undergo genome reduction due to genetic drift, rather than purifying selection. [18] [1] Genetic drift is caused by small and effective populations within a microbial community, rather than large and dominating populations. [1] In this case, DNA mutations happen by chance, and thus often lead to maladaptive genome degradation and lower overall fitness. [18] Rather than losing non-coding DNA regions or extraneous genes to increase fitness during replication, they lose certain "core" metabolic genes that may now be supplemented by their host, symbiont, or environment. [18] Since their genome reduction is less dependent on fitness, pseudogenes are frequent in these organisms. [1] They also typically undergo low rates of horizontal gene transfer (HGT).

Variation in genome sizes of viruses, prokaryotes, and eukaryotes Genome size vs protein count.svg
Variation in genome sizes of viruses, prokaryotes, and eukaryotes

Viruses

Viral genomes resemble prokaryotic genomes in that they have very few non-coding regions. [19] They are, however, significantly smaller than prokaryotic genomes. While viruses are obligate intracellular parasites, viral genomes are considered streamlined due to the strong purifying selection that occurs when the virus has successfully infected a host. [20] [21] During the initial phase of an infection, there is a large bottleneck for the virus population which allows for more genetic diversity, but due to the rapid replication of these viruses, the population size is restored quickly and the diversity within the population is reduced. [21]

RNA viruses in particular are known to have exceptionally small genomes. [22] This is at least in part due to the fact that they have overlapping genes. [22] By reducing their genome size, they increase their fitness due to faster replication. [22] The virus will then be able to increase population size more rapidly with faster replication rates.

Eukaryotes - birds

Genomic streamlining has been used to explain certain eukaryotic genome sizes as well, particularly bird genomes. Larger genomes require a larger nucleus, which typically translates to a larger cell size. [23] For this reason, many bird genomes have also been under selective pressure to decrease in size. [23] [24] Flying with a larger mass due to larger cells is more energetically expensive than with a smaller mass. [24]

Related Research Articles

<i>Prochlorococcus</i> Genus of bacteria

Prochlorococcus is a genus of very small (0.6 μm) marine cyanobacteria with an unusual pigmentation. These bacteria belong to the photosynthetic picoplankton and are probably the most abundant photosynthetic organism on Earth. Prochlorococcus microbes are among the major primary producers in the ocean, responsible for a large percentage of the photosynthetic production of oxygen. Prochlorococcus strains, called ecotypes, have physiological differences enabling them to exploit different ecological niches. Analysis of the genome sequences of Prochlorococcus strains show that 1,273 genes are common to all strains, and the average genome size is about 2,000 genes. In contrast, eukaryotic algae have over 10,000 genes.

<i>Candidatus Pelagibacter communis</i> Species of bacterium

"Candidatus Pelagibacter", with the single species "Ca. P. communis", was isolated in 2002 and given a specific name, although it has not yet been described as required by the bacteriological code. It is an abundant member of the SAR11 clade in the phylum Alphaproteobacteria. SAR11 members are highly dominant organisms found in both salt and fresh water worldwide and were originally known only from their rRNA genes, first identified in the Sargasso Sea in 1990 by Stephen Giovannoni's laboratory at Oregon State University and later found in oceans worldwide. "Ca. P. communis" and its relatives may be the most abundant organisms in the ocean, and quite possibly the most abundant bacteria in the entire world. It can make up about 25% of all microbial plankton cells, and in the summer they may account for approximately half the cells present in temperate ocean surface water. The total abundance of "Ca. P. communis" and relatives is estimated to be about 2 × 1028 microbes.

<span class="mw-page-title-main">Genome size</span> Amount of DNA contained in a genome

Genome size is the total amount of DNA contained within one copy of a single complete genome. It is typically measured in terms of mass in picograms or less frequently in daltons, or as the total number of nucleotide base pairs, usually in megabases. One picogram is equal to 978 megabases. In diploid organisms, genome size is often used interchangeably with the term C-value.

<span class="mw-page-title-main">Alphaproteobacteria</span> Class of bacteria

Alphaproteobacteria is a class of bacteria in the phylum Pseudomonadota. The Magnetococcales and Mariprofundales are considered basal or sister to the Alphaproteobacteria. The Alphaproteobacteria are highly diverse and possess few commonalities, but nevertheless share a common ancestor. Like all Proteobacteria, its members are gram-negative, although some of its intracellular parasitic members lack peptidoglycan and are consequently gram variable.

<i>Synechococcus</i> Genus of bacteria

Synechococcus is a unicellular cyanobacterium that is very widespread in the marine environment. Its size varies from 0.8 to 1.5 μm. The photosynthetic coccoid cells are preferentially found in well–lit surface waters where it can be very abundant. Many freshwater species of Synechococcus have also been described.

<span class="mw-page-title-main">Cyanophage</span> Virus that infects cyanobacteria

Cyanophages are viruses that infect cyanobacteria, also known as Cyanophyta or blue-green algae. Cyanobacteria are a phylum of bacteria that obtain their energy through the process of photosynthesis. Although cyanobacteria metabolize photoautotrophically like eukaryotic plants, they have prokaryotic cell structure. Cyanophages can be found in both freshwater and marine environments. Marine and freshwater cyanophages have icosahedral heads, which contain double-stranded DNA, attached to a tail by connector proteins. The size of the head and tail vary among species of cyanophages. Cyanophages infect a wide range of cyanobacteria and are key regulators of the cyanobacterial populations in aquatic environments, and may aid in the prevention of cyanobacterial blooms in freshwater and marine ecosystems. These blooms can pose a danger to humans and other animals, particularly in eutrophic freshwater lakes. Infection by these viruses is highly prevalent in cells belonging to Synechococcus spp. in marine environments, where up to 5% of cells belonging to marine cyanobacterial cells have been reported to contain mature phage particles.

<span class="mw-page-title-main">Bacteria</span> Domain of microorganisms

Bacteria are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were among the first life forms to appear on Earth, and are present in most of its habitats. Bacteria inhabit soil, water, acidic hot springs, radioactive waste, and the deep biosphere of Earth's crust. Bacteria play a vital role in many stages of the nutrient cycle by recycling nutrients and the fixation of nitrogen from the atmosphere. The nutrient cycle includes the decomposition of dead bodies; bacteria are responsible for the putrefaction stage in this process. In the biological communities surrounding hydrothermal vents and cold seeps, extremophile bacteria provide the nutrients needed to sustain life by converting dissolved compounds, such as hydrogen sulphide and methane, to energy. Bacteria also live in mutualistic, commensal and parasitic relationships with plants and animals. Most bacteria have not been characterised and there are many species that cannot be grown in the laboratory. The study of bacteria is known as bacteriology, a branch of microbiology.

Mycoplasma laboratorium or Synthia refers to a synthetic strain of bacterium. The project to build the new bacterium has evolved since its inception. Initially the goal was to identify a minimal set of genes that are required to sustain life from the genome of Mycoplasma genitalium, and rebuild these genes synthetically to create a "new" organism. Mycoplasma genitalium was originally chosen as the basis for this project because at the time it had the smallest number of genes of all organisms analyzed. Later, the focus switched to Mycoplasma mycoides and took a more trial-and-error approach.

Ultramicrobacteria are bacteria that are smaller than 0.1 μm3 under all growth conditions. This term was coined in 1981, describing cocci in seawater that were less than 0.3 μm in diameter. Ultramicrobacteria have also been recovered from soil and appear to be a mixture of Gram-positive, Gram-negative and cell-wall-lacking species. Ultramicrobacteria possess a relatively high surface-area-to-volume ratio due to their small size, which aids in growth under oligotrophic conditions. The relatively small size of ultramicrobacteria also enables parasitism of larger organisms; some ultramicrobacteria have been observed to be obligate or facultative parasites of various eukaryotes and prokaryotes. One factor allowing ultramicrobacteria to achieve their small size seems to be genome minimization such as in the case of the ultramicrobacterium P. ubique whose small 1.3 Mb genome is seemingly devoid of extraneous genetic elements like non-coding DNA, transposons, extrachromosomal elements etc. However, genomic data from ultramicrobacteria is lacking since the study of ultramicrobacteria, like many other prokaryotes, is hindered by difficulties in cultivating them.

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

Archaea is a domain of organisms. Traditionally, Archaea only included its prokaryotic members, but this sense has been found to be paraphyletic, as eukaryotes are now known to have evolved from archaea. Even though the domain Archaea includes eukaryotes, the term "archaea" in English still generally refers specifically to prokaryotic members of Archaea. Archaea were initially classified as bacteria, receiving the name archaebacteria, but this term has fallen out of use.

Evolution of cells refers to the evolutionary origin and subsequent evolutionary development of cells. Cells first emerged at least 3.8 billion years ago approximately 750 million years after Earth was formed.

<span class="mw-page-title-main">Pelagibacterales</span> Order of bacteria

The Pelagibacterales are an order in the Alphaproteobacteria composed of free-living marine bacteria that make up roughly one in three cells at the ocean's surface. Overall, members of the Pelagibacterales are estimated to make up between a quarter and a half of all prokaryotic cells in the ocean.

<span class="mw-page-title-main">Genome evolution</span> Process by which a genome changes in structure or size over time

Genome evolution is the process by which a genome changes in structure (sequence) or size over time. The study of genome evolution involves multiple fields such as structural analysis of the genome, the study of genomic parasites, gene and ancient genome duplications, polyploidy, and comparative genomics. Genome evolution is a constantly changing and evolving field due to the steadily growing number of sequenced genomes, both prokaryotic and eukaryotic, available to the scientific community and the public at large.

Bacterial genomes are generally smaller and less variant in size among species when compared with genomes of eukaryotes. Bacterial genomes can range in size anywhere from about 130 kbp to over 14 Mbp. A study that included, but was not limited to, 478 bacterial genomes, concluded that as genome size increases, the number of genes increases at a disproportionately slower rate in eukaryotes than in non-eukaryotes. Thus, the proportion of non-coding DNA goes up with genome size more quickly in non-bacteria than in bacteria. This is consistent with the fact that most eukaryotic nuclear DNA is non-gene coding, while the majority of prokaryotic, viral, and organellar genes are coding. Right now, we have genome sequences from 50 different bacterial phyla and 11 different archaeal phyla. Second-generation sequencing has yielded many draft genomes ; third-generation sequencing might eventually yield a complete genome in a few hours. The genome sequences reveal much diversity in bacteria. Analysis of over 2000 Escherichia coli genomes reveals an E. coli core genome of about 3100 gene families and a total of about 89,000 different gene families. Genome sequences show that parasitic bacteria have 500–1200 genes, free-living bacteria have 1500–7500 genes, and archaea have 1500–2700 genes. A striking discovery by Cole et al. described massive amounts of gene decay when comparing Leprosy bacillus to ancestral bacteria. Studies have since shown that several bacteria have smaller genome sizes than their ancestors did. Over the years, researchers have proposed several theories to explain the general trend of bacterial genome decay and the relatively small size of bacterial genomes. Compelling evidence indicates that the apparent degradation of bacterial genomes is owed to a deletional bias.

An overlapping gene is a gene whose expressible nucleotide sequence partially overlaps with the expressible nucleotide sequence of another gene. In this way, a nucleotide sequence may make a contribution to the function of one or more gene products. Overlapping genes are present in and a fundamental feature of both cellular and viral genomes. The current definition of an overlapping gene varies significantly between eukaryotes, prokaryotes, and viruses. In prokaryotes and viruses overlap must be between coding sequences but not mRNA transcripts, and is defined when these coding sequences share a nucleotide on either the same or opposite strands. In eukaryotes, gene overlap is almost always defined as mRNA transcript overlap. Specifically, a gene overlap in eukaryotes is defined when at least one nucleotide is shared between the boundaries of the primary mRNA transcripts of two or more genes, such that a DNA base mutation at any point of the overlapping region would affect the transcripts of all genes involved. This definition includes 5′ and 3′ untranslated regions (UTRs) along with introns.

The Pelagibacteraceae are a family in the Alphaproteobacteria composed of free-living marine bacteria.

Auxiliary metabolic genes (AMGs) are found in many bacteriophages but originated in bacterial cells. AMGs modulate host cell metabolism during infection so that the phage can replicate more efficiently. For instance, bacteriophages that infect the abundant marine cyanobacteria Synechococcus and Prochlorococcus (cyanophages) carry AMGs that have been acquired from their immediate host as well as more distantly-related bacteria. Cyanophage AMGs support a variety of functions including photosynthesis, carbon metabolism, nucleic acid synthesis and metabolism. AMGs also have broader ecological impacts beyond their host including their influence on biogeochemical cycling.

A plastid is a membrane-bound organelle found in plants, algae and other eukaryotic organisms that contribute to the production of pigment molecules. Most plastids are photosynthetic, thus leading to color production and energy storage or production. There are many types of plastids in plants alone, but all plastids can be separated based on the number of times they have undergone endosymbiotic events. Currently there are three types of plastids; primary, secondary and tertiary. Endosymbiosis is reputed to have led to the evolution of eukaryotic organisms today, although the timeline is highly debated.

The Black Queen hypothesis (BQH) is a reductive evolution theory which seeks to explain how natural selection can drive gene loss. In a microbial community, different members may have genes which produce certain chemicals or resources in a "leaky fashion" making them accessible to other members of that community. If this resource is available to certain members of a community in a way that allows them to sufficiently access that resource without generating it themselves, these other members in the community may lose the biological function involved in producing that chemical. Put another way, the black queen hypothesis is concerned with the conditions under which it is advantageous to lose certain biological functions. By accessing resources without the need to generate it themselves, these microbes conserve energy and streamline their genomes to enable faster replication.

<span class="mw-page-title-main">Marine viruses</span> Viruses found in marine environments

Marine viruses are defined by their habitat as viruses that are found in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. Viruses are small infectious agents that can only replicate inside the living cells of a host organism, because they need the replication machinery of the host to do so. They can infect all types of life forms, from animals and plants to microorganisms, including bacteria and archaea.

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