skip to main content

Title: Insights into ecological role of a new deltaproteobacterial order Candidatus Acidulodesulfobacterales by metagenomics and metatranscriptomics

Several abundant but yet uncultivated bacterial groups exist in extreme iron- and sulfur-rich environments, and the physiology, biodiversity, and ecological roles of these bacteria remain a mystery. Here we retrieved four metagenome-assembled genomes (MAGs) from an artificial acid mine drainage (AMD) system, and propose they belong to a new deltaproteobacterial order, Candidatus Acidulodesulfobacterales. The distribution pattern of Ca. Acidulodesulfobacterales in AMDs across Southeast China correlated strongly with ferrous iron. Reconstructed metabolic pathways and gene expression profiles showed that they were likely facultatively anaerobic autotrophs capable of nitrogen fixation. In addition to dissimilatory sulfate reduction, encoded by dsrAB, dsrD, dsrL, and dsrEFH genes, these microorganisms might also oxidize sulfide, depending on oxygen concentration and/or oxidation reduction potential. Several genes with homology to those involved in iron metabolism were also identified, suggesting their potential role in iron cycling. In addition, the expression of abundant resistance genes revealed the mechanisms of adaptation and response to the extreme environmental stresses endured by these organisms in the AMD environment. These findings shed light on the distribution, diversity, and potential ecological role of the new order Ca. Acidulodesulfobacterales in nature.

more » « less
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
The ISME Journal
Medium: X Size: p. 2044-2057
["p. 2044-2057"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    The orderSulfolobaleswas one of the first named Archaeal lineages, with globally distributed members from terrestrial thermal acid springs (pH < 4;T > 65°C). TheSulfolobalesrepresent broad metabolic capabilities, ranging from lithotrophy, based on inorganic iron and sulfur biotransformations, to autotrophy, to chemoheterotrophy in less acidophilic species. Components of the 3‐hydroxypropionate/4‐hydroxybutyrate carbon fixation cycle, as well as sulfur oxidation, are nearly universally conserved, although dissimilatory sulfur reduction and disproportionation (Acidianus,StygiolobusandSulfurisphaera) and iron oxidation (Acidianus,Metallosphaera,Sulfurisphaera,SulfuracidifexandSulfodiicoccus) are limited to fewer lineages. Lithotrophic marker genes appear more often in highly acidophilic lineages. Despite the presence of facultative anaerobes and one confirmed obligate anaerobe, oxidase complexes (fox,sox,doxand a new putative cytochrome bd) are prevalent in many species (even facultative/obligate anaerobes), suggesting a key role for oxygen among theSulfolobales. The presence offoxgenes tracks with a putative antioxidant OsmC family peroxiredoxin, an indicator of oxidative stress derived from mixing reactive metals and oxygen. Extreme acidophily appears to track inversely with heterotrophy but directly with lithotrophy. Recent phylogenetic re‐organization efforts are supported by the comparative genomics here, although several changes are proposed, including the expansion of the genusSaccharolobus.

    more » « less
  2. Abstract

    Fusobacterium varium has been generally overlooked in cattle rumen microbiome studies relative to the presumably more abundant liver abscess-causing Fusobacterium necrophorum. However, F. varium was found to be more abundant in the rumen fluid of cattle and under culture conditions tailored to enrich F. necrophorum. Using near-full length 16S ribosomal ribonucleic acid sequencing, we demonstrate that F. varium grows under restrictive conditions commonly used to enumerate F. necrophorum, suggesting that previous F. necrophorum abundance assessment may have been inaccurate and that F. varium may be an underestimated member of the ruminal bacterial community. Fusobacterium varium were not as susceptible as F. necrophorum to in-feed antibiotics conventionally used in feedlots. Exposure to tylosin, the current gold standard for liver abscess reduction strategies in cattle, consistently hindered growth of the F. necrophorum strains tested by over 67% (P < 0.05) relative to the unexposed control. In contrast, F. varium strains were totally or highly resistant (0%–13% reduction in maximum yield, P < 0.05). Monensin, an ionophore antibiotic, had greater inhibitory activity against F. necrophorum than F. varium. Finally, preliminary genomic analysis of two F. varium isolates from the rumen revealed the presence of virulence genes related to those of pathogenic human F. varium isolates associated with active invasion of mammalian cells. The data presented here encourage further investigation into the ecological role of F. varium within the bovine rumen and potential role in liver abscess development, and proactive interventions.

    more » « less
  3. Abstract

    The Ediacara biota features the rise of macroscopic complex life immediately before the Cambrian explosion. One of the most abundant and widely distributed elements of the Ediacara biota is the discoidal fossilAspidella, which is interpreted as a subsurface holdfast possibly anchoring a frondose epibenthic organism. It is a morphologically simple fossil preserved mainly in siliciclastic rocks, which are unsuitable for comprehensive stable isotope geochemical analyses to decipher its taphonomy and paleoecology. In this regard, three‐dimensionally preservedAspidellafossils from upper Ediacaran limestones of the Khatyspyt Formation in the Olenek Uplift of northern Siberia offer a rare opportunity to leverage geochemistry for insights into their taphonomy and paleoecology. To take advantage of this opportunity, we analyzed δ13Ccarb, δ18Ocarb, δ13Corg, δ34Spyr, and iron speciation of the KhatyspytAspidellafossils and surrounding sediment matrix in order to investigate whether they hosted microbial symbionts, how they were fossilized, and the redox conditions of their ecological environments.Aspidellaholdfasts and surrounding sediment matrix show indistinguishable δ13Corgvalues, suggesting they did not host and derive significant amount of nutrients from microbial symbionts such as methanogens, methylotrophs, or sulfide‐oxidizing bacteria. δ13Ccarb, δ18Ocarb, and δ34Spyrdata, along with petrographic observations, suggest that microbial sulfate reduction facilitated the preservation ofAspidellaby promoting early authigenic calcite cementation in the holdfasts before matrix cementation and sediment compaction. Iron speciation data are equivocal, largely because of the low total iron concentrations. However, consideration of published sulfur isotope and biomarker data suggests thatAspidellalikely lived in non‐euxinic waters. It is possible thatAspidellawas an opportunistic organism, colonizing the seafloor in large numbers when paleoenvironments were favorable. This study demonstrates that geochemical data of Ediacaran fossils preserved in limestones can offer important insights into the taphonomy and paleoecology of these enigmatic organisms living on the eve of the Cambrian explosion.

    more » « less
  4. Abstract

    Natural populations are characterized by abundant genetic diversity driven by a range of different types of mutation. The tractability of sequencing complete genomes has allowed new insights into the variable composition of genomes, summarized as a species pan‐genome. These analyses demonstrate that many genes are absent from the first reference genomes, whose analysis dominated the initial years of the genomic era. Our field now turns towards understanding the functional consequence of these highly variable genomes. Here, we analysed weighted gene coexpression networks from leaf transcriptome data for drought response in the purple false bromeBrachypodium distachyonand the differential expression of genes putatively involved in adaptation to this stressor. We specifically asked whether genes with variable “occupancy” in the pan‐genome – genes which are either present in all studied genotypes or missing in some genotypes – show different distributions among coexpression modules. Coexpression analysis united genes expressed in drought‐stressed plants into nine modules covering 72 hub genes (87 hub isoforms), and genes expressed under controlled water conditions into 13 modules, covering 190 hub genes (251 hub isoforms). We find that low occupancy pan‐genes are under‐represented among several modules, while other modules are over‐enriched for low‐occupancy pan‐genes. We also provide new insight into the regulation of drought response inB. distachyon, specifically identifying one module with an apparent role in primary metabolism that is strongly responsive to drought. Our work shows the power of integrating pan‐genomic analysis with transcriptomic data using factorial experiments to understand the functional genomics of environmental response.

    more » « less
  5. Rudi, Knut (Ed.)
    ABSTRACT Cyanobacterial harmful algal blooms (cyanoHABs) degrade freshwater ecosystems globally. Microcystis aeruginosa often dominates cyanoHABs and produces microcystin (MC), a class of hepatotoxins that poses threats to human and animal health. Microcystin toxicity is influenced by distinct structural elements across a diversity of related molecules encoded by variant mcy operons. However, the composition and distribution of mcy operon variants in natural blooms remain poorly understood. Here, we characterized the variant composition of mcy genes in western Lake Erie Microcystis blooms from 2014 and 2018. Sampling was conducted across several spatial and temporal scales, including different bloom phases within 2014, extensive spatial coverage on the same day (2018), and frequent, autonomous sampling over a 2-week period (2018). Mapping of metagenomic and metatranscriptomic sequences to reference sequences revealed three Microcystis mcy genotypes: complete (all genes present [ mcyA–J ]), partial (truncated mcyA , complete mcyBC , and missing mcyD–J ), and absent (no mcy genes). We also detected two different variants of mcyB that may influence the production of microcystin congeners. The relative abundance of these genotypes was correlated with pH and nitrate concentrations. Metatranscriptomic analysis revealed that partial operons were, at times, the most abundant genotype and expressed in situ , suggesting the potential biosynthesis of truncated products. Quantification of genetic divergence between genotypes suggests that the observed strains are the result of preexisting heterogeneity rather than de novo mutation during the sampling period. Overall, our results show that natural Microcystis populations contain several cooccurring mcy genotypes that dynamically shift in abundance spatiotemporally via strain succession and likely influence the observed diversity of the produced congeners. IMPORTANCE Cyanobacteria are responsible for producing microcystins (MCs), a class of potent and structurally diverse toxins, in freshwater systems around the world. While microcystins have been studied for over 50 years, the diversity of their chemical forms and how this variation is encoded at the genetic level remain poorly understood, especially within natural populations of cyanobacterial harmful algal blooms (cyanoHABs). Here, we leverage community DNA and RNA sequences to track shifts in mcy genes responsible for producing microcystin, uncovering the relative abundance, expression, and variation of these genes. We studied this phenomenon in western Lake Erie, which suffers annually from cyanoHAB events, with impacts on drinking water, recreation, tourism, and commercial fishing. 
    more » « less