Salinity-triggered compositional and metabolic responses of autotrophic prokaryotes in Tibetan lacustrine sediments

Abstract Background Autotrophic prokaryotes are crucial participants in the global carbon cycle, and autotrophic carbon fixation contributes approximately 50% of the global net primary production in aquatic ecosystems per year. Salinity is a prominent regulator structuring microbial communities in diverse aquatic ecosystems. However, little information is available regarding the compositional and physiological response of autotrophic microbial communities to salinity change. Here, we used genome-resolved metagenomics to study autotrophic microbial communities in 25 Tibetan lacustrine sediments with a salinity gradient (from 0.54‰ to 82.6‰). Results117 metagenome-assembled genomes (MAGs) with carbon fixation potential belonging to 12 phyla were retrieved, of which approximately 21% were not affiliated with the known orders, suggesting taxonomically diverse autotrophic assemblages in sediments. The total abundance of these putative autotrophs decreased significantly with increasing salinity, and the variation of sediment autotrophic communities was mainly driven by salinity, pH and TOC. Notably, a change in the predominant lineage from Betaproteobacteria to Deltaproteobacteria was observed along the salinity gradient, and the dominant pathway for carbon fixation shifted from the Calvin-Benson-Bassham (CBB) cycle to more energy efficient Wood-Lungdahl (WL) pathway with glycolysis from Entner-Doudoroff to more exergonic Embden-Meyerhof-Parnas, demonstrating that the physiological efficiency increases from freshwater to hypersaline autotrophic communities. Metabolic inference revealed major links for carbon fixation to the oxidation of reduced sulfur compounds, ferrous iron and carbon monoxide, denitrification and nitrogen fixation in these MAGs, as well as the occurrence of dissimilatory sulfate reduction and the WL pathway dominating hypersaline sediments, greatly extending the understanding of metabolic versatility and diverse ecological niches of autotrophic microorganisms. Conclusions This study provided a systematic attempt to characterize the response of carbon fixation pathways to salinity and the knowledge essential for revealing ecological roles of autotrophic prokaryotes in aquatic habitats. These findings suggest with increased salinity, physiological efficiency of the autotrophic community increases, which has important implications for understanding the carbon budget in aquatic ecosystems.

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Transcriptional Activities of the Microbial Consortium Living with the Marine Nitrogen-Fixing Cyanobacterium Trichodesmium Reveal Potential Roles in Community-Level Nitrogen Cycling

Applied and Environmental Microbiology ◽

10.1128/aem.02026-17 ◽

2017 ◽

Vol 84 (1) ◽

Cited By ~ 6

Author(s):

Michael D. Lee ◽

Eric A. Webb ◽

Nathan G. Walworth ◽

Fei-Xue Fu ◽

Noelle A. Held ◽

...

Keyword(s):

Gene Expression ◽

Nitrogen Fixation ◽

Microbial Communities ◽

Nitrogen Cycling ◽

Carbon Fixation ◽

Community Respiration ◽

Ecological Niches ◽

Nitrogen Fixing ◽

Content Type ◽

Globally Distributed

ABSTRACTTrichodesmiumis a globally distributed cyanobacterium whose nitrogen-fixing capability fuels primary production in warm oligotrophic oceans. Like many photoautotrophs,Trichodesmiumserves as a host to various other microorganisms, yet little is known about how this associated community modulates fluxes of environmentally relevant chemical species into and out of the supraorganismal structure. Here, we utilized metatranscriptomics to examine gene expression activities of microbial communities associated withTrichodesmium erythraeum(strain IMS101) using laboratory-maintained enrichment cultures that have previously been shown to harbor microbial communities similar to those of natural populations. In enrichments maintained under two distinct CO2concentrations for ∼8 years, the community transcriptional profiles were found to be specific to the treatment, demonstrating a restructuring of overall gene expression had occurred. Some of this restructuring involved significant increases in community respiration-related transcripts under elevated CO2, potentially facilitating the corresponding measured increases in host nitrogen fixation rates. Particularly of note, in both treatments, community transcripts involved in the reduction of nitrate, nitrite, and nitrous oxide were detected, suggesting the associated organisms may play a role in colony-level nitrogen cycling. Lastly, a taxon-specific analysis revealed distinct ecological niches of consistently cooccurring major taxa that may enable, or even encourage, the stable cohabitation of a diverse community withinTrichodesmiumconsortia.IMPORTANCETrichodesmiumis a genus of globally distributed, nitrogen-fixing marine cyanobacteria. As a source of new nitrogen in otherwise nitrogen-deficient systems, these organisms help fuel carbon fixation carried out by other more abundant photoautotrophs and thereby have significant roles in global nitrogen and carbon cycling. Members of theTrichodesmiumgenus tend to form large macroscopic colonies that appear to perpetually host an association of diverse interacting microbes distinct from the surrounding seawater, potentially making the entire assemblage a unique miniature ecosystem. Since its first successful cultivation in the early 1990s, there have been questions about the potential interdependencies betweenTrichodesmiumand its associated microbial community and whether the host's seemingly enigmatic nitrogen fixation schema somehow involved or benefited from its epibionts. Here, we revisit these old questions with new technology and investigate gene expression activities of microbial communities living in association withTrichodesmium.

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Weak Influence of Paleoenvironmental Conditions on the Subsurface Biosphere of Lake Ohrid over the Last 515 ka

Microorganisms ◽

10.3390/microorganisms8111736 ◽

2020 ◽

Vol 8 (11) ◽

pp. 1736

Author(s):

Camille Thomas ◽

Alexander Francke ◽

Hendrik Vogel ◽

Bernd Wagner ◽

Daniel Ariztegui

Keyword(s):

Microbial Communities ◽

Lacustrine Sediments ◽

Environmental Parameters ◽

Strong Relationship ◽

Low Energy ◽

Rrna Gene ◽

Deep Biosphere ◽

Lake Ohrid ◽

Metabolic Versatility ◽

The Impact

Lacustrine sediments are widely used to investigate the impact of climatic change on biogeochemical cycling. In these sediments, subsurface microbial communities are major actors of this cycling but can also affect the sedimentary record and overprint the original paleoenvironmental signal. We therefore investigated the subsurface microbial communities of the oldest lake in Europe, Lake Ohrid (North Macedonia, Albania), to assess the potential connection between microbial diversity and past environmental change using 16S rRNA gene sequences. Along the upper ca. 200 m of the DEEP site sediment record spanning ca. 515 thousand years (ka), our results show that Atribacteria, Bathyarchaeia and Gammaproteobacteria structured the community independently from each other. Except for the latter, these taxa are common in deep lacustrine and marine sediments due to their metabolic versatility adapted to low energy environments. Gammaproteobacteria were often co-occurring with cyanobacterial sequences or soil-related OTUs suggesting preservation of ancient DNA from the water column or catchment back to at least 340 ka, particularly in dry glacial intervals. We found significant environmental parameters influencing the overall microbial community distribution, but no strong relationship with given phylotypes and paleoclimatic signals or sediment age. Our results support a weak recording of early diagenetic processes and their actors by bulk prokaryotic sedimentary DNA in Lake Ohrid, replaced by specialized low-energy clades of the deep biosphere and a marked imprint of erosional processes on the subsurface DNA pool of Lake Ohrid.

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Metabolic Modeling of Pectobacterium parmentieri SCC3193 Provides Insights into Metabolic Pathways of Plant Pathogenic Bacteria

Microorganisms ◽

10.3390/microorganisms7040101 ◽

2019 ◽

Vol 7 (4) ◽

pp. 101 ◽

Cited By ~ 5

Author(s):

Sabina Zoledowska ◽

Luana Presta ◽

Marco Fondi ◽

Francesca Decorosi ◽

Luciana Giovannetti ◽

...

Keyword(s):

In Silico ◽

Pathogenic Bacteria ◽

Metabolic Modeling ◽

Metabolic Model ◽

Metabolic Adaptation ◽

Ecological Niches ◽

Plant Colonization ◽

Phenotypic Data ◽

Plant Pathogenic Bacteria ◽

Metabolic Versatility

Understanding plant–microbe interactions is crucial for improving plants’ productivity and protection. Constraint-based metabolic modeling is one of the possible ways to investigate the bacterial adaptation to different ecological niches and may give insights into the metabolic versatility of plant pathogenic bacteria. We reconstructed a raw metabolic model of the emerging plant pathogenic bacterium Pectobacterium parmentieri SCC3193 with the use of KBase. The model was curated by using inParanoind and phenotypic data generated with the use of the OmniLog system. Metabolic modeling was performed through COBRApy Toolbox v. 0.10.1. The curated metabolic model of P. parmentieri SCC3193 is highly reliable, as in silico obtained results overlapped up to 91% with experimental data on carbon utilization phenotypes. By mean of flux balance analysis (FBA), we predicted the metabolic adaptation of P. parmentieri SCC3193 to two different ecological niches, relevant for the persistence and plant colonization by this bacterium: soil and the rhizosphere. We performed in silico gene deletions to predict the set of essential core genes for this bacterium to grow in such environments. We anticipate that our metabolic model will be a valuable element for defining a set of metabolic targets to control infection and spreading of this plant pathogen.

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The keystone species of Precambrian deep bedrock biosphere belong to <i>Burkholderiales</i> and <i>Clostridiales</i>

Biogeosciences Discussions ◽

10.5194/bgd-12-18103-2015 ◽

2015 ◽

Vol 12 (21) ◽

pp. 18103-18150 ◽

Cited By ~ 3

Author(s):

L. Purkamo ◽

M. Bomberg ◽

R. Kietäväinen ◽

H. Salavirta ◽

M. Nyyssönen ◽

...

Keyword(s):

Microbial Communities ◽

Carbon Fixation ◽

Keystone Species ◽

Carbon Assimilation ◽

Sugar Metabolism ◽

Archaeal Community ◽

Amino Sugar ◽

Amplicon Sequencing ◽

Fracture Zones ◽

Crystalline Bedrock

Abstract. The bacterial and archaeal community composition and the possible carbon assimilation processes and energy sources of microbial communities in oligotrophic, deep, crystalline bedrock fractures is yet to be resolved. In this study, intrinsic microbial communities from six fracture zones from 180–2300 m depths in Outokumpu bedrock were characterized using high-throughput amplicon sequencing and metagenomic prediction. Comamonadaceae-, Anaerobrancaceae- and Pseudomonadaceae-related OTUs form the core community in deep crystalline bedrock fractures in Outokumpu. Archaeal communities were mainly composed of Methanobacteraceae-affiliating OTUs. The predicted bacterial metagenomes showed that pathways involved in fatty acid and amino sugar metabolism were common. In addition, relative abundance of genes coding the enzymes of autotrophic carbon fixation pathways in predicted metagenomes was low. This indicates that heterotrophic carbon assimilation is more important for microbial communities of the fracture zones. Network analysis based on co-occurrence of OTUs revealed the keystone genera of the microbial communities belonging to Burkholderiales and Clostridiales. Bacterial communities in fractures resemble those found from oligotrophic, hydrogen-enriched environments. Serpentinization reactions of ophiolitic rocks in Outokumpu assemblage may provide a source of energy and organic carbon compounds for the microbial communities in the fractures. Sulfate reducers and methanogens form a minority of the total microbial communities, but OTUs forming these minor groups are similar to those found from other deep Precambrian terrestrial bedrock environments.

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Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations

mSystems ◽

10.1128/msystems.01196-20 ◽

2021 ◽

Vol 6 (3) ◽

Author(s):

Sarahi L. Garcia ◽

Maliheh Mehrshad ◽

Moritz Buck ◽

Jackson M. Tsuji ◽

Josh D. Neufeld ◽

...

Keyword(s):

Carbon Fixation ◽

Carbon Sources ◽

Natural Populations ◽

Freshwater Ecosystems ◽

Electron Donors ◽

Functional Ecology ◽

Lake Ecosystems ◽

Tropical Regions ◽

Metabolic Versatility ◽

Globally Distributed

ABSTRACT Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on the functional ecology and local adaptations of Chlorobia members came from isolates and merely 26 sequenced genomes that may not adequately represent natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-amplified genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs or “species”). Of the 71 mOTUs, 57 were classified within the genus Chlorobium, and these mOTUs represented up to ∼60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed, whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many lacked genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insight into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems. IMPORTANCE The reconstruction of genomes from metagenomes has helped explore the ecology and evolution of environmental microbiota. We applied this approach to 274 metagenomes collected from diverse freshwater habitats that spanned oxic and anoxic zones, sampling seasons, and latitudes. We demonstrate widespread and abundant distributions of planktonic Chlorobia-associated bacteria in hypolimnetic waters of stratified freshwater ecosystems and show they vary in their capacities to use different electron donors. Having photoautotrophic potential, these Chlorobia members could serve as carbon sources that support metalimnetic and hypolimnetic food webs.

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Microbial dark carbon fixation fueled by nitrate enrichment

10.1101/2021.08.24.457596 ◽

2021 ◽

Author(s):

Joseph H. Vineis ◽

Ashley N. Bulseco ◽

Jennifer L. Bowen

Keyword(s):

Microbial Communities ◽

Marine Sediments ◽

Salt Marshes ◽

Carbon Fixation ◽

Niche Partitioning ◽

Coastal Marine Sediments ◽

Functional Relationships ◽

Coastal Marine ◽

Dark Carbon Fixation ◽

The Impact

Anthropogenic nitrate amendment to coastal marine sediments can increase rates of heterotrophic mineralization and autotrophic dark carbon fixation (DCF). DCF may be favored in sediments where organic matter is biologically unavailable, leading to a microbial community supported by chemoautotrophy. Niche partitioning among DCF communities and adaptations for nitrate metabolism in coastal marine sediments remain poorly characterized, especially within salt marshes. We used genome-resolved metagenomics, phylogenetics, and comparative genomics to characterize the potential niche space, phylogenetic relationships, and adaptations important to microbial communities within nitrate enriched sediment. We found that nitrate enrichment of sediment from discrete depths between 0-25 cm supported both heterotrophs and chemoautotrophs that use sulfur oxidizing denitrification to drive the Calvin-Benson-Bassham (CBB) or reductive TCA (rTCA) DCF pathways. Phylogenetic reconstruction indicated that the nitrate enriched community represented a small fraction of the phylogenetic diversity contained in coastal marine environmental genomes, while pangenomics revealed close evolutionary and functional relationships with DCF microbes in other oligotrophic environments. These results indicate that DCF can support coastal marine microbial communities and should be carefully considered when estimating the impact of nitrate on carbon cycling in these critical habitats.

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Composition and predictive functional analysis of bacterial communities in the surface seawater of the Changjiang Estuary

10.7287/peerj.preprints.3079v1 ◽

2017 ◽

Author(s):

Dong-Mei Wu ◽

Jian-Xin Wang ◽

Xiao-Hui Liu ◽

Ying-Ping Fan ◽

Ran Jiang ◽

...

Keyword(s):

Dissolved Oxygen ◽

Microbial Communities ◽

Bacterial Communities ◽

High Throughput Sequencing ◽

Carbon Fixation ◽

Oxygen Demand ◽

Environmental Parameters ◽

Changjiang Estuary ◽

Surface Seawater ◽

The Changjiang Estuary

The objective of this study was to characterize the structure and function of microbial communities in surface seawater from the Changjiang Estuary and adjacent areas, China. Sample water was collected at 12 sites and environmental parameters were measured. Community structure was analyzed using high-throughput sequencing of 16S rDNA genes. Predictive metagenomic approach was used to predict the function of bacterial communities. Result showed that sample site A0102 had the highest bacterial abundance and diversity. The heatmap indicated that different samples could be clustered into six groups. Phylogenetic analysis showed that Proteobacteria was the predominant phylum in all samples, followed by Bacteroidetes and Actinobacteria. Alphaproteobacteria and Gammaproteobacteria were the dominant classes. The analysis of predictive metagenomic showed carbon fixation pathways in prokaryotes, nitrogen metabolism, carbon fixation in photosynthetic organisms, photosynthesis and polycyclic aromatic hydrocarbon degradation were enriched in all samples. Redundancy analysis (RDA) identified that dissolved oxygen (DO) and PO43– concentration had positive correlations with the bacterial communities while chemical oxygen demand (COD), dissolved oxygen (DO) and PO43– concentration were significantly associated with microbial functional diversity. This study adds to our knowledge of functional and taxonomic composition of microbial communities.

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Composition changes of phototrophic microbial communities along the salinity gradient in the solar saltern evaporation ponds of Eilat, Israel

Hydrobiologia ◽

10.1007/s10750-009-9936-0 ◽

2009 ◽

Vol 636 (1) ◽

pp. 77-88 ◽

Cited By ~ 12

Author(s):

Klára Řeháková ◽

Eliška Zapomělová ◽

Ondřej Prášil ◽

Jana Veselá ◽

Hana Medová ◽

...

Keyword(s):

Microbial Communities ◽

Salinity Gradient ◽

Solar Saltern ◽

Evaporation Ponds ◽

Composition Changes

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Inorganic carbon fixation in ice-covered lakes of the McMurdo Dry Valleys

Antarctic Science ◽

10.1017/s0954102019000075 ◽

2019 ◽

Vol 31 (3) ◽

pp. 123-132 ◽

Cited By ~ 1

Author(s):

Trista J. Vick-Majors ◽

John C. Priscu

Keyword(s):

Aquatic Ecosystems ◽

Inorganic Carbon ◽

Carbon Fixation ◽

Dry Valleys ◽

Ammonia Oxidizers ◽

Fixed Carbon ◽

Carbon Supply ◽

Gain Energy ◽

Photosynthetic Microorganisms ◽

Dark Carbon Fixation

AbstractInorganic carbon fixation, usually mediated by photosynthetic microorganisms, is considered to form the base of the food chain in aquatic ecosystems. In high-latitude lakes, lack of sunlight owing to seasonal solar radiation limits the activity of photosynthetic plankton during the polar winter, causing respiration-driven demand for carbon to exceed supply. Here, we show that inorganic carbon fixation in the dark, driven by organisms that gain energy from chemical reactions rather than sunlight (chemolithoautotrophs), provides a significant influx of fixed carbon to two permanently ice-covered lakes (Fryxell and East Bonney). Fryxell, which has higher biomass per unit volume of water, had higher rates of inorganic dark carbon fixation by chemolithoautotrophs than East Bonney (trophogenic zone average 1.0 µg C l−1 d−1vs 0.08 µg C l−1 d−1, respectively). This contribution from dark carbon fixation was partly due to the activity of ammonia oxidizers, which are present in both lakes. Despite the potential importance of new carbon input by chemolithoautotrophic activity, both lakes remain net heterotrophic, with respiratory demand for carbon exceeding supply. Dark carbon fixation increased the ratio of new carbon supply to respiratory demand from 0.16 to 0.47 in Fryxell, and from 0.14 to 0.22 in East Bonney.

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Environmental microbiology: biodegradation

Philosophical Transactions of the Royal Society of London Series B Biological Sciences ◽

10.1098/rstb.1982.0063 ◽

1982 ◽

Vol 297 (1088) ◽

pp. 575-597 ◽

Cited By ~ 36

Keyword(s):

Microbial Communities ◽

Metabolic Activity ◽

Metabolic Pathways ◽

Environmental Microbiology ◽

Single Species ◽

Natural Compounds ◽

Synthetic Compounds ◽

Metabolic Versatility ◽

Xenobiotic Compounds

A genuinely new dimension to microbiology concerns the fate of synthetic compounds dispersed throughout the biosphere, with xenobiotic compounds representing a major challenge to the metabolic versatility of microorganisms. While microbial bio-degradation of many of these compounds proceeds by the activity of single species of microorganisms, this paper develops the argument that microbial communities function by synergistic mechanisms to effect the breakdown of many of these compounds. The degradation of some compounds, especially xenobiotic compounds, depends on the use of gratuitous metabolic pathways evolved for natural compounds, which in many instances may be evolved through the combined metabolic activity of two or more microorganisms. The role of plasmid coded pathways is also considered in the context of the evolution of novel pathways.

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