The phylum Acidobacteria is one of the most widespread and abundant on the planet, yet remarkably our knowledge of the role of these diverse organisms in the functioning of terrestrial ecosystems remains surprisingly rudimentary. This blatant knowledge gap stems to a large degree from the difficulties associated with the cultivation of these bacteria by classical means. Given the phylogenetic breadth of the Acidobacteria , which is similar to the metabolically diverse Proteobacteria , it is clear that detailed and functional descriptions of acidobacterial assemblages are necessary. Fortunately, recent advances are providing a glimpse into the ecology of members of the phylum Acidobacteria.
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The phylum Acidobacteria is one of the most widespread and abundant on the planet, yet remarkably our knowledge of the role of these diverse organisms in the functioning of terrestrial ecosystems remains surprisingly rudimentary.
This blatant knowledge gap stems to a large degree from the difficulties associated with the cultivation of these bacteria by classical means. Given the phylogenetic breadth of the Acidobacteria , which is similar to the metabolically diverse Proteobacteria , it is clear that detailed and functional descriptions of acidobacterial assemblages are necessary.
Fortunately, recent advances are providing a glimpse into the ecology of members of the phylum Acidobacteria. These include novel cultivation and enrichment strategies, genomic characterization and analyses of metagenomic DNA from environmental samples.
Here, we couple the data from these complementary approaches for a better understanding of their role in the environment, thereby providing some initial insights into the ecology of this important phylum. All cultured acidobacterial type species are heterotrophic, and members of subdivisions 1, 3, and 4 appear to be more versatile in carbohydrate utilization.
Genomic and metagenomic data predict a number of ecologically relevant capabilities for some acidobacteria, including the ability to: use of nitrite as N source, respond to soil macro-, micro nutrients and soil acidity, express multiple active transporters, degrade gellan gum and produce exopolysaccharide EPS. Although these predicted properties allude to a competitive life style in soil, only very few of these prediction shave been confirmed via physiological studies.
The increased availability of genomic and physiological information, coupled to distribution data in field surveys and experiments, should direct future progress in unraveling the ecology of this important but still enigmatic phylum.
Although the Acidobacteria were only recognized as a phylum relatively recently, their abundance across a range of ecosystems, especially soils, has demanded research into their ecology. However, despite their high abundance and diversity, we still have relatively little information regarding the actual activities and ecology of members of this phylum, a shortcoming that can be attributed to a large extent to the difficulties in cultivating the majority of acidobacteria and their poor coverage in bacterial culture collections Bryant et al.
However, environmental surveys have provided insight into some the environmental factors that may drive acidobacteria dynamics, such as pH and nutrients Fierer et al. In , the first sequenced genomes of acidobacteria strains became available, providing preliminary genetic insights into the potential physiology and environment functions of several members of this phylum Ward et al. In these first genomic studies, five aspects of physiological received particular attention: i carbon usage, ii nitrogen assimilation, iii metabolism of iron, iv antimicrobials, and v abundance of transporters.
Besides genome sequencing of cultivated isolates, addition information regarding genomic properties of acidobacteria has been derived from metagenomics studies Liles et al.
In this review, we couple the complementary data coming from physiological, genomic and metagenomics studies to seek a better understanding of the role of Acidobacteria in the environment, thereby providing some initial insights into the ecology of this important phylum. We aim to not only give a more complete picture of the current knowledge of Acidobacteria , but also seek to provide a solid base for future experiments geared toward gaining a better understanding of the ecological roles played by members of this phylum.
The introduction of molecular biological strategies into microbial ecology over the past decades has yielded a new perspective on the breadth and vastness of microbial diversity.
The phylum of the Acidobacteria is one of the bacterial lineages that has profited most from the cultivation-independent interrogation of environmental samples. Indeed, in the past two decades, this phylum has grown from being virtually unknown to being recognized as one of the most abundant and diverse on Earth. Based on phylogenetic analysis of 16S rRNA gene sequences, the Acidobacteria phylum raised from the originally described four to six subdivisions Kuske et al.
Currently there are 26 accepted subdivisions Barns et al. The first recognized strain and species of the phylum Acidobacteria was Acidobacterium capsulatum obtained from an acid mine drainage in Japan Kishimoto and Tano, ; Kishimoto et al. Although the second isolate belonging to this phylum was Holophaga foetida first described in , it was not initially recognized as related to Acidobacteria capsulatum.
Instead, it was thought to belong to the phylum Proteobacteria Liesack et al. A few years later, a closely related bacterium named Geothrix fermentans was isolated Coates et al. Since these isolates were very distantly related to A. Currently Acidobacteria phylum has 26 subdivisions based on the extremely broad diversity of acidobacterial populations found in uranium-contaminated soils Barns et al.
The vast majority of isolates cultivated to date are affiliated with acidobacteria subdivision 1 Class Acidobacteriia.
They are all heterotrophic, most species are aerobic or microaerophilic and some species Telmatobacter bradus, Acidobacterium capsulatum are facultative anaerobic bacteria Pankratov et al. Members of subdivisions 3, 4, 8 currently Class Holophagae , 10, and 23 are heterotrophic as well. Thermotomaculum subdivision 10 and Thermoanaerobaculum subdivision 23 are thermophilic anaerobic bacteria Izumi et al.
Chloracidobacterium thermophilum is photoheterotrophic Bryant et al. Subdivision 8 contains one aerobic Acanthopleuribacter and two strictly anaerobic isolates Holophaga and Geothrix. There are reports of acidobacteria isolates belonging to subdivisions 2 and 6, but they still do not have valid taxonomic names Sait et al.
Subdivisions 1 and 3 of the phylum Acidobacteria together with thermophilic Thermoanaerobacter species are capable of biosynthesizing total fatty acids lipid Damste et al. In addition, there are the genome sequences of Koribacter and Solibacter , but there is little information on their physiology. Dendrogram showing the general characteristics of Acidobacteria type species, only.
There were a total of positions in the final dataset. Acidobacterium capsulatum was originally described as an aerobic bacteria, but later it was demonstrated a weak anaerobic growth by fermentation Pankratov et al. ND, not determined. Changes in the traditional methods for culturing bacteria from soils have significantly improved the isolation of Acidobacteria strains in recent years. These new strategies involve the use of relatively low concentration of nutrients, non-traditional sources of carbon or complex polysaccharides Janssen et al.
It is suggested that raising the CO 2 concentration may not only better mimic the CO 2 concentrations typically found in soils, but may also decrease medium pH, thereby benefiting certain members of the acidobacteria, especially moderate acidophilic strains belonging to subdivision 1 Sait et al.
This combination of strategies seems to enrich not only for Acidobacteria but for many other groups of slow-growing bacteria.
The association of a molecular technique such as the high-throughput plate-wash PCR Stevenson et al. Once Acidobacteria isolation under low nutrient conditions is achieved, strains can often be transferred to richer media e. Despite the importance of these recent advances in cultivation methods, further improvements are clearly needed since only eight of a total of 26 subdivisions are known to have representatives in culture. A large number of Acidobacteria isolates have been recovered from the Australian soil Ellin bank Janssen et al.
However, many of these bacteria have not yet been fully characterized and still do not possess valid taxonomical names. Further, micro-cultivation strategies combined with single-cell sequencing should provide access to new acidobacterial genomes, and in turn this genomic information may help to inform future isolation efforts as cultivation is still required for most physiological characterizations.
The first comparative genome analysis between of A. Since then, the number of acidobacterial genomes being sequenced remains rather limited. Currently, there are 10 published genomes of Acidobacteria available: five subdivision 1 Ward et al.
Below, we summarize some of the major findings revealed via the currently available acidobacterial genome sequences linked to physiological studies. Among all the physiological aspects revealed by genomics, carbohydrate metabolism has been studied most widely, which is not surprising considering that carbon usage is one of the physiological requirements for the description of new species in taxonomic studies.
The ability to use glucose and xylose makes sense given the fact that cellulose or xylan are often the major carbon sources in the culture media most typically used for the isolation of Acidobacteria. In addition, these bacteria were able to use most of the tested oligosaccharides, although maltose and cellobiose were not able to support growth of Edaphobacter species.
Interestingly, the majority of subdivision 1 species were unable to use fucose or sorbose, carbohydrates that are only minor components of plant cell walls and rather scarce in soil Li et al. Usage of carbon sources by Acidobacteria in culture-based experiments with type strain species. A positive score was recorded if at least one species within a genus is able to use a respective sugar.
A Acidobacteria subdivision 1. B Acidobacteria subdivisions 3 and 4. Usage of carbon source obtained from original references that described each of the type species, in order of publication: Kishimoto et al.
In contrast, chitin usage has not yet been demonstrated for any member of Acidobacteria subdivision 1. Similarly, cellulose was another substrate predicted to be degraded by Acidobacteria genome annotation.
However, only Telmatobacter bradus subdivision 1 has been demonstrated to be able to use crystalline cellulose Pankratov et al. Terracidiphilus gabretensis produces extracellular enzymes implicated in the degradation of plant-derived biopolymers what was confirmed by genome analysis by the presence of enzymatic machinery required for organic matter decomposition Garcia-Fraile et al.
In contrast to Acidobacteria from subdivision 1, members of subdivision 4 are able to use chitin as a carbon source Foesel et al. Most of the Acidobacteria subdivisions 1, 3, or 4 examined to date is unable to use carboxymethyl cellulose, but there is evidence that Aridibacter kavangonensis subdivision 4 is able to utilize micro-crystalline cellulose Huber et al.
Although it is still premature to draw general conclusions related to the degradation of these abundant polysaccharides by Acidobacteria in nature, xylan degradation has been broadly demonstrated, which may play a role in plant cell wall degradation Pankratov et al.
The discrepancies between genome predictions and observed activities may stem from our ability to provide cultivation conditions that lead to the expression of the target activities. Alternatively, current automatic genome annotation pipelines may not successfully differentiate genes involved for instance in chitin and cellulose degradation from genes involved in the degradation of other glycosyl hydrolases, such as xylan.
Systematic studies on the degradation of cellulose by Acidobacteria grown on different culture conditions may help to test the hypothesis of gene regulation by sugars present in the media, for example. On the other hand, it has been reported that in bacteria many genes involved in cellulose degradation may be involved in the infection of plant cells or in the synthesis of bacterial cellulose Koeck et al.
Enzymatic activities observed in Acidobacteria have usually been detected using commercial kits with chromogenic substrates. Galactosidases are enzymes involved in the hydrolysis of galactose-containing sugars, while beta galactosidades are involved in the degradation of lactose. Since all genera of Acidobacteria subdivision 1 are able to use lactose, it is not surprising to find this enzyme included in their enzymatic profile.
Glucosidases are involved in the degradation of polysaccharides, especially cellulose and starch. Enzymes encoding genes of polysaccharide degradation EC. The comparisons were done using IMG: the integrated microbial genomes database and comparative analysis system. Janssen et al. In contrast to agar, which is obtained from seaweed, gellan gum is a substrate that is produced and degraded by soil bacteria.
At least two species of Acidobacteria have demonstrated ability to use gellan gum: Telmatobacter bradus and Bryocella elongata. Members of Acidobacteria subdivision 1 were reported to be able to use the monosaccharides rhamnose and glucose. However, the in silico comparison of 10 available genomes, offered no evidence of gellan lyase EC 4.
The investigation of the enzymatic pathway for gellan gum degradation may merit further investigation, since this is a bacterial polysaccharide. Therefore, in addition to the possible metabolism of polysaccharides derived from plants, the usage of gellan gum suggests an interaction with other soil bacteria Dedysh et al.
Nitrite reduction was observed in all three genomes reported in , and nitrate reduction in two of the initially analyzed genomes Ward et al. Nitrate reduction has been investigated in almost all members of subdivision 1, with the exception of Acidobacterium and Acidicapsa. Among all Granulicella species, G. Among other subdivisions, only Geothrix fermentans subdivision 8 was shown to be able to reduce nitrate.
This organism is an iron reducer that can use nitrate as an alternative electron acceptor. All of these Acidobacteria were able to use yeast extract that, in addition to ammonium, may be a preferred nitrogen source Coates et al.
The presence of the nirA gene, which encodes nitrate reductase, also appears to be limited to subdivision 1, suggesting that members of this subdivision may reduce nitrate to nitrite by the assimilatory pathway, which is further reduced to ammonia and assimilated into glutamate. Nevertheless, the direct uptake of ammonium seems likely as all genomes described to date appear to contain genes for the ammonia transporter channel Amt family TC 1.
Genes encoding dinitrogenase, a heterotetramer of the proteins NifD and NifK genes nifD and nifK , respectively and dinitrogenase reductase, a homodimer of the protein NifH gene nifH , were found only in the genome of H.
Ammonia monooxygenase amo and nitrous-oxide reductase nosZ genes were not found in any of the available genomes.
NCBI: Taxonomy. Acidobacteria capsulatum A. The flagella themselves are peritrichous or found all over the surface of the cell. Another characteristic of this organism is the presence of high amounts of exopolysaccharide coating the cells from soil isolates 2. This contributes to the competitiveness of A. Members of this phylum are presumably ubiquitous in soil environments and A.
The phylum Acidobacteria is one of the most widespread and abundant on the planet, yet remarkably our knowledge of the role of these diverse organisms in the functioning of terrestrial ecosystems remains surprisingly rudimentary. This blatant knowledge gap stems to a large degree from the difficulties associated with the cultivation of these bacteria by classical means. Given the phylogenetic breadth of the Acidobacteria , which is similar to the metabolically diverse Proteobacteria , it is clear that detailed and functional descriptions of acidobacterial assemblages are necessary. Fortunately, recent advances are providing a glimpse into the ecology of members of the phylum Acidobacteria. These include novel cultivation and enrichment strategies, genomic characterization and analyses of metagenomic DNA from environmental samples.