Organisms capable of autotrophic metabolism assimilate inorganic carbon into organic carbon. They form an integral part of ecosystems by making an otherwise unavailable form of carbon available to ...other organisms, a central component of the global carbon cycle. For many years, the doctrine prevailed that the Calvin-Benson-Bassham (CBB) cycle is the only biochemical autotrophic CO2 fixation pathway of significance in the ocean. However, ecological, biochemical, and genomic studies carried out over the last decade have not only elucidated new pathways but also shown that autotrophic carbon fixation via pathways other than the CBB cycle can be significant. This has ramifications for our understanding of the carbon cycle and energy flow in the ocean. Here, we review the recent discoveries in the field of autotrophic carbon fixation, including the biochemistry and evolution of the different pathways, as well as their ecological relevance in various oceanic ecosystems.
A novel bacterium, strain EPR55-1T, was isolated from a deep-sea hydrothermal vent on the East Pacific Rise. The cells were motile rods. Growth was observed at temperatures between 50 and 60°C ...(optimum, 60°C), at pH values between 5.4 and 8.6 (optimum, pH 6.6) and in the presence of 2.4-3.2% (w/v) NaCl (optimum, 2.4%). The isolate used molecular hydrogen as its sole electron donor, carbon dioxide as its sole carbon source, ammonium as its sole nitrogen source, and thiosulfate, sulfite (0.01 to 0.001%, w/v) or elemental sulfur as its sole sulfur source. Nitrate, nitrous oxide (33%, v/v), thiosulfate, molecular oxygen (0.1%, v/v) or elemental sulfur could serve as the sole electron acceptor to support growth. Phylogenetic analyses based on both 16S rRNA gene sequences and whole genome sequences indicated that strain EPR55-1T belonged to the family Nitratiruptoraceae of the class "Campylobacteria", but it had the distinct phylogenetic relationship with the genus Nitratiruptor. On the basis of the physiological and molecular characteristics of the isolate, the name Nitrosophilus alvini gen. nov. sp. nov. is proposed, with EPR55-1T as the type strain (= JCM 32893T = KCTC 15925T). In addition, it is shown that "Nitratiruptor labii" should be transferred to the genus Nitrtosophilus; the name Nitrosophilus labii comb. nov. (JCM 34002T = DSM 111345T) is proposed for this organism. Furthermore, 16S rRNA gene-based and genome-based analyses showed that Cetia pacifica is phylogenetically associated with Caminibacter species. We therefore propose the reclassification of Cetia pacifica as Caminibacter pacificus comb. nov. (DSM 27783T = JCM 19563T). Additionally, AAI thresholds for genus classification and the reclassification of subordinate taxa within "Campylobacteria" are also evaluated, based on the analyses using publicly available genomes of all the campylobacterial species.
Genome sequencing enhances our understanding of the biological world by providing blueprints for the evolutionary and functional diversity that shapes the biosphere. However, microbial genomes that ...are currently available are of limited phylogenetic breadth, owing to our historical inability to cultivate most microorganisms in the laboratory. We apply single-cell genomics to target and sequence 201 uncultivated archaeal and bacterial cells from nine diverse habitats belonging to 29 major mostly uncharted branches of the tree of life, so-called 'microbial dark matter'. With this additional genomic information, we are able to resolve many intra- and inter-phylum-level relationships and to propose two new superphyla. We uncover unexpected metabolic features that extend our understanding of biology and challenge established boundaries between the three domains of life. These include a novel amino acid use for the opal stop codon, an archaeal-type purine synthesis in Bacteria and complete sigma factors in Archaea similar to those in Bacteria. The single-cell genomes also served to phylogenetically anchor up to 20% of metagenomic reads in some habitats, facilitating organism-level interpretation of ecosystem function. This study greatly expands the genomic representation of the tree of life and provides a systematic step towards a better understanding of biological evolution on our planet.
It has been proposed that early bacteria, or even the last universal common ancestor of all cells, were thermophilic. However, research on the origin and evolution of thermophily is hampered by the ...difficulties associated with the isolation of deep-branching thermophilic microorganisms in pure culture. Here, we isolate a deep-branching thermophilic bacterium from a deep-sea hydrothermal vent, using a two-step cultivation strategy ("Subtraction-Suboptimal", StS) designed to isolate rare organisms. The bacterium, which we name Zhurongbacter thermophilus 3DAC, is a sulfur-reducing heterotroph that is phylogenetically related to Coprothermobacterota and other thermophilic bacterial groups, forming a clade that seems to represent a major, early-diverging bacterial lineage. The ancestor of this clade might be a thermophilic, strictly anaerobic, motile, hydrogen-dependent, and mixotrophic bacterium. Thus, our study provides insights into the early evolution of thermophilic bacteria.
Below the seafloor at deep-sea hot springs, mixing of geothermal fluids with seawater supports a potentially vast microbial ecosystem. Although the identity of subseafloor microorganisms is largely ...known, their effect on deep-ocean biogeochemical cycles cannot be predicted without quantitative measurements of their metabolic rates and growth efficiency. Here, we report on incubations of subseafloor fluids under in situ conditions that quantitatively constrain subseafloor primary productivity, biomass standing stock, and turnover time. Single-cell-based activity measurements and 16S rRNA-gene analysis showed that Campylobacteria dominated carbon fixation and that oxygen concentration and temperature drove niche partitioning of closely related phylotypes. Our data reveal a very active subseafloor biosphere that fixes carbon at a rate of up to 321 μg C·L−1·d−1, turns over rapidly within tens of hours, rivals the productivity of chemosynthetic symbioses above the seafloor, and significantly influences deep-ocean biogeochemical cycling.
The
is the fifth validly described class of the phylum Proteobacteria, known primarily for clinical relevance and for chemolithotrophy in various terrestrial and marine environments, including ...deep-sea hydrothermal vents. As 16S rRNA gene repositories have expanded and protein marker analysis become more common, the phylogenetic placement of this class has become less certain. A number of recent analyses of the bacterial tree of life using both 16S rRNA and concatenated marker gene analyses have failed to recover the
as monophyletic with all other classes of Proteobacteria. In order to address this issue, we investigated the phylogenetic placement of this class in the bacterial domain using 16S and 23S rRNA genes, as well as 120 single-copy marker proteins. Single- and concatenated-marker trees were created using a data set of 4,170 bacterial representatives, including 98
. Phylogenies were inferred under a variety of tree building methods, with sequential jackknifing of outgroup phyla to ensure robustness of phylogenetic affiliations under differing combinations of bacterial genomes. Based on the assessment of nearly 300 phylogenetic tree topologies, we conclude that the continued inclusion of
within the Proteobacteria is not warranted, and that this group should be reassigned to a novel phylum for which we propose the name Epsilonbacteraeota (phyl. nov.). We further recommend the reclassification of the order
(
) to a novel class within this phylum and a number of subordinate changes to ensure consistency with the genome-based phylogeny. Phylogenomic analysis of 658 genomes belonging to the newly proposed Epsilonbacteraeota suggests that the ancestor of this phylum was an autotrophic, motile, thermophilic chemolithotroph that likely assimilated nitrogen from ammonium taken up from the environment or generated from environmental nitrate and nitrite by employing a variety of functional redox modules. The emergence of chemoorganoheterotrophic lifestyles in several Epsilonbacteraeota families is the result of multiple independent losses of various ancestral chemolithoautotrophic pathways. Our proposed reclassification of this group resolves an important anomaly in bacterial systematics and ensures that the taxonomy of Proteobacteria remains robust, specifically as genome-based taxonomies become more common.
Chemoautotrophy at Deep-Sea Vents SIEVERT, STEFAN M.; VETRIANI, COSTANTINO
Oceanography,
03/2012, Letnik:
25, Številka:
1
Journal Article
Recenzirano
Odprti dostop
Chemolithoautotrophic microorganisms are at the nexus of hydrothermal systems by effectively transferring the energy from the geothermal source to the higher trophic levels. While the validity of ...this conceptual framework is well established at this point, there are still significant gaps in our understanding of the microbiology and biogeochemistry of deep-sea hydrothermal systems. Important questions in this regard are: (1) How much, at what rates, and where in the system is organic carbon being produced? (2) What are the dominant autotrophs, where do they reside, and what is the relative importance of free-swimming, biofilm-forming, and symbiotic microbes? (3) Which metabolic pathways are they using to conserve energy and to fix carbon? (4) How does community-wide gene expression in fluid and biofilm communities compare? and (5) How efficiently is the energy being utilized, transformed into biomass, and transferred to higher trophic levels? In particular, there is currently a notable lack of process-oriented studies that would allow an assessment of the larger role of these ecosystems in global biogeochemical cycles. By combining the presently available powerful "omic" and single-cell tools with thermodynamic modeling, experimental approaches, and new in situ instrumentation to measure rates and concentrations, it is now possible to bring our understanding of these truly fascinating ecosystems to a new level and to place them in a quantitative framework and thus a larger global context.
Coastal climate adaptation strategies are needed to build salt marsh resiliency and maintain critical ecosystem services in response to impacts caused by climate change. Although resident microbial ...communities perform crucial biogeochemical cycles for salt marsh functioning, their response to restoration practices is still understudied. One promising restoration strategy is the placement of sand or sediment onto the marsh platform to increase marsh resiliency. A previous study examined the above- and below-ground structure, soil carbon dioxide emissions, and pore water constituents in Spartina alterniflora-vegetated natural marsh sediments and sand-amended sediments at varying inundation regimes. Here, we analyzed samples from the same experiment to test the effect of sand-amendments on the microbial communities after 5 months. Along with the previously observed changes in biogeochemistry, sand amendments drastically modified the bacterial communities, decreasing richness and diversity. The dominant sulfur-cycling bacterial community found in natural sediments was replaced by one dominated by iron oxidizers and aerobic heterotrophs, the abundance of which correlated with higher CO2-flux. In particular, the relative abundance of iron-oxidizing Zetaproteobacteria increased in the sand-amended sediments, possibly contributing to acidification by the formation of iron oxyhydroxides. Our data suggest that the bacterial community structure can equilibrate if the inundation regime is maintained within the optimal range for S. alterniflora. While long-term effects of changes in bacterial community on the growth of S. alterniflora are not clear, our results suggest that analyzing the microbial community composition could be a useful tool to monitor climate adaptation and restoration efforts.
The rapidly increasing availability of complete bacterial genomes has created new opportunities for reconstructing bacterial evolution, but it has also highlighted the difficulty to fully understand ...the genomic and functional variations occurring among different lineages. Using the class Epsilonproteobacteria as a case study, we investigated the composition, flexibility, and function of its pan-genomes. Models were constructed to extrapolate the expansion of pan-genomes at three different taxonomic levels. The results show that, for Epsilonproteobacteria the seemingly large genome variations among strains of the same species are less noticeable when compared with groups at higher taxonomic ranks, indicating that genome stability is imposed by the potential existence of taxonomic boundaries. The analyses of pan-genomes has also defined a set of universally conserved core genes, based on which a phylogenetic tree was constructed to confirm that thermophilic species from deep-sea hydrothermal vents represent the most ancient lineages of Epsilonproteobacteria. Moreover, by comparing the flexible genome of a chemoautotrophic deep-sea vent species to (1) genomes of species belonging to the same genus, but inhabiting different environments, and (2) genomes of other vent species, but belonging to different genera, we were able to delineate the relative importance of lineage-specific versus niche-specific genes. This result not only emphasizes the overall importance of phylogenetic proximity in shaping the variable part of the genome, but also highlights the adaptive functions of niche-specific genes. Overall, by modeling the expansion of pan-genomes and analyzing core and flexible genes, this study provides snapshots on how the complex processes of gene acquisition, conservation, and removal affect the evolution of different species, and contribute to the metabolic diversity and versatility of Epsilonproteobacteria.
Molecular surveys of low temperature deep-sea hydrothermal vent fluids have shown that
(previously
) often dominate the microbial community and that three genera,
,
, and
, frequently coexist. In ...this study, we used replicated radiocarbon incubations of deep-sea hydrothermal fluids to investigate activity of each genus under three experimental conditions. To quantify genus-specific radiocarbon incorporation, we used newly designed oligonucleotide probes for
,
, and
to quantify their activity using catalyzed-reporter deposition fluorescence
hybridization (CARD-FISH) combined with fluorescence-activated cell sorting. All three genera actively fixed CO
in short-term (∼ 20 h) incubations, but responded differently to the additions of nitrate and oxygen. Oxygen additions had the largest effect on community composition, and caused a pronounced shift in community composition at the amplicon sequence variant (ASV) level after only 20 h of incubation. The effect of oxygen on carbon fixation rates appeared to depend on the initial starting community. The presented results support the hypothesis that these chemoautotrophic genera possess functionally redundant core metabolic capabilities, but also reveal finer-scale differences in growth likely reflecting adaptation of physiologically-distinct phylotypes to varying oxygen concentrations
. Overall, our study provides new insights into how oxygen controls community composition and total chemoautotrophic activity, and underscores how quickly deep-sea vent microbial communities respond to disturbances.
Sulfidic environments worldwide are often dominated by sulfur-oxidizing, carbon-fixing
. Environmental factors associated with this group's dominance are now understood, but far less is known about the ecology and physiology of members of subgroups of chemoautotrophic
. In this study, we used a novel method to differentiate the genus-specific chemoautotrophic activity of three subtypes of
In combination with evidence from microscopic counts, chemical consumption/production during incubations, and DNA-based measurements, our data show that oxygen concentration affects both community composition and chemoautotrophic function
. These results help us better understand factors controlling microbial diversity at deep-sea hydrothermal vents, and provide first-order insights into the ecophysiological differences between these distinct microbial taxa.
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