scholarly journals Acquisition of the arginine deiminase system benefits epiparasitic Saccharibacteria and their host bacteria in a mammalian niche environment

2022 ◽  
Vol 119 (2) ◽  
pp. e2114909119
Author(s):  
Jing Tian ◽  
Daniel R. Utter ◽  
Lujia Cen ◽  
Pu-Ting Dong ◽  
Wenyuan Shi ◽  
...  

Saccharibacteria are a group of widespread and genetically diverse ultrasmall bacteria with highly reduced genomes that belong to the Candidate Phyla Radiation. Comparative genomic analyses suggest convergent evolution of key functions enabling the adaptation of environmental Saccharibacteria to mammalian microbiomes. Currently, our understanding of this environment-to-mammal niche transition within Saccharibacteria and their obligate episymbiotic association with host bacteria is limited. Here, we identified a complete arginine deiminase system (ADS), found in further genome streamlined mammal-associated Saccharibacteria but missing in their environmental counterparts, suggesting acquisition during environment-to-mammal niche transition. Using TM7x, the first cultured Saccharibacteria strain from the human oral microbiome and its host bacterium Actinomyces odontolyticus, we experimentally tested the function and impact of the ADS. We demonstrated that by catabolizing arginine and generating adenosine triphosphate, the ADS allows metabolically restrained TM7x to maintain higher viability and infectivity when disassociated from the host bacterium. Furthermore, the ADS protects TM7x and its host bacterium from acid stress, a condition frequently encountered within the human oral cavity due to bacterial metabolism of dietary carbohydrates. Intriguingly, with a restricted host range, TM7x forms obligate associations with Actinomyces spp. lacking the ADS but not those carrying the ADS, suggesting the acquired ADS may also contribute to partner selection for cooperative episymbiosis within a mammalian microbiome. These data present experimental characterization of a mutualistic interaction between TM7x and their host bacteria, and illustrate the benefits of acquiring a novel pathway in the transition of Saccharibacteria to mammalian microbiomes.

Author(s):  
Christine He ◽  
Ray Keren ◽  
Michael Whittaker ◽  
Ibrahim F. Farag ◽  
Jennifer Doudna ◽  
...  

AbstractCandidate Phyla Radiation (CPR) bacteria and DPANN archaea are uncultivated, small-celled symbionts often detected in groundwater. However, variations in CPR/DPANN organism abundance, distribution, taxonomic diversity, and degree/nature of host association with groundwater chemistry remain understudied. Here, we performed genome-resolved metagenomic characterization of one agriculturally-impacted and seven pristine groundwater microbial communities in California, recovering 746 dereplicated CPR and DPANN genomes. Our finding of up to 31% CPR bacteria and 4% DPANN archaea in the pristine sites, which serve as local sources of drinking water, may hold health relevance, given growing awareness of the presence of CPR/DPANN organisms in human microbiomes and their association with disease. There is little species-level genome overlap across groundwater sites, indicating that CPR and DPANN communities are highly differentiated according to host populations and physicochemical conditions. Cryo-TEM imaging and genomic analyses indicate that CPR growth may be stimulated by attachment to the surface of host cells, and identified CPR and DPANN lineages with particularly prevalent and/or resilient host cell attachment. These results establish the huge but site-specific diversity of CPR bacteria and DPANN archaea coexisting with diverse hosts in groundwater aquifers, and raise important questions about potential impacts on human health.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Justin D Lormand ◽  
Soo-Kyoung Kim ◽  
George A Walters-Marrah ◽  
Bryce A Brownfield ◽  
J Christopher Fromme ◽  
...  

RNA degradation is fundamental for cellular homeostasis. The process is carried out by various classes of endolytic and exolytic enzymes that together degrade an RNA polymer to mono-ribonucleotides. Within the exoribonucleases, nano-RNases play a unique role as they act on the smallest breakdown products and hence catalyze the final steps in the process. We recently showed that oligoribonuclease (Orn) acts as a dedicated diribonucleotidase, defining the ultimate step in RNA degradation that is crucial for cellular fitness (Kim et al., 2019). Whether such a specific activity exists in organisms that lack Orn-type exoribonucleases remained unclear. Through quantitative structure-function analyses, we show here that NrnC-type RNases share this narrow substrate length preference with Orn. Although NrnC and Orn employ similar structural features that distinguish these two classes of dinucleotidases from other exonucleases, the key determinants for dinucleotidase activity are realized through distinct structural scaffolds. The structures, together with comparative genomic analyses of the phylogeny of DEDD-type exoribonucleases, indicate convergent evolution as the mechanism of how dinucleotidase activity emerged repeatedly in various organisms. The evolutionary pressure to maintain dinucleotidase activity further underlines the important role these analogous proteins play for cell growth.


Open Biology ◽  
2021 ◽  
Vol 11 (2) ◽  
pp. 200359
Author(s):  
Núria Ros-Rocher ◽  
Alberto Pérez-Posada ◽  
Michelle M. Leger ◽  
Iñaki Ruiz-Trillo

How animals evolved from a single-celled ancestor, transitioning from a unicellular lifestyle to a coordinated multicellular entity, remains a fascinating question. Key events in this transition involved the emergence of processes related to cell adhesion, cell–cell communication and gene regulation. To understand how these capacities evolved, we need to reconstruct the features of both the last common multicellular ancestor of animals and the last unicellular ancestor of animals. In this review, we summarize recent advances in the characterization of these ancestors, inferred by comparative genomic analyses between the earliest branching animals and those radiating later, and between animals and their closest unicellular relatives. We also provide an updated hypothesis regarding the transition to animal multicellularity, which was likely gradual and involved the use of gene regulatory mechanisms in the emergence of early developmental and morphogenetic plans. Finally, we discuss some new avenues of research that will complement these studies in the coming years.


2020 ◽  
Vol 99 (6) ◽  
pp. 685-694 ◽  
Author(s):  
B. Bor ◽  
A.J. Collins ◽  
P.P. Murugkar ◽  
S. Balasubramanian ◽  
T.T. To ◽  
...  

Oral microbiome research has moved from asking “Who’s there?” to “What are they doing?” Understanding what microbes “do” involves multiple approaches, including obtaining genomic information and examining the interspecies interactions. Recently we isolated a human oral Saccharibacteria (TM7) bacterium, HMT-952, strain TM7x, which is an ultrasmall parasite of the oral bacterium Actinomyces odontolyticus. The host-parasite interactions, such as phage-bacterium or Saccharibacteria–host bacterium, are understudied areas with large potential for insight. The Saccharibacteria phylum is a member of Candidate Phyla Radiation, a large lineage previously devoid of cultivated members. However, expanding our understanding of Saccharibacteria-host interactions requires examining multiple phylogenetically distinct Saccharibacteria-host pairs. Here we report the isolation of 3 additional Saccharibacteria species from the human oral cavity in binary coculture with their bacterial hosts. They were obtained by filtering ultrasmall Saccharibacteria cells free of other larger bacteria and inoculating them into cultures of potential host bacteria. The binary cocultures obtained could be stably passaged and studied. Complete closed genomes were obtained and allowed full genome analyses. All have small genomes (<1 Mb) characteristic of parasitic species and dramatically limited de novo synthetic pathway capabilities but include either restriction modification or CRISPR-Cas systems as part of an innate defense against foreign DNA. High levels of gene synteny exist among Saccharibacteria species. Having isolates growing in coculture with their hosts allowed time course studies of growth and parasite-host interactions by phase contrast, fluorescence in situ hybridization, and scanning electron microscopy. The cells of the 4 oral Saccharibacteria species are ultrasmall and could be seen attached to their larger Actinobacteria hosts. Parasite attachment appears to lead to host cell death and lysis. The successful cultivation of Saccharibacteria species has significantly expanded our understanding of these ultrasmall Candidate Phyla Radiation bacteria.


2021 ◽  
Vol 7 (17) ◽  
pp. eabd2274
Author(s):  
Elaine E. Guevara ◽  
Timothy H. Webster ◽  
Richard R. Lawler ◽  
Brenda J. Bradley ◽  
Lydia K. Greene ◽  
...  

Sifakas (genus Propithecus) are critically endangered, large-bodied diurnal lemurs that eat leaf-based diets and show corresponding anatomical and microbial adaptations to folivory. We report on the genome assembly of Coquerel’s sifaka (P. coquereli) and the resequenced genomes of Verreaux’s (P. verreauxi), the golden-crowned (P. tattersalli), and the diademed (P. diadema) sifakas. We find high heterozygosity in all sifakas compared with other primates and endangered mammals. Demographic reconstructions nevertheless suggest declines in effective population size beginning before human arrival on Madagascar. Comparative genomic analyses indicate pervasive accelerated evolution in the ancestral sifaka lineage affecting genes in several complementary pathways relevant to folivory, including nutrient absorption and xenobiotic and fatty acid metabolism. Sifakas show convergent evolution at the level of the pathway, gene family, gene, and amino acid substitution with other folivores. Although sifakas have relatively generalized diets, the physiological challenges of habitual folivory likely led to strong selection.


2017 ◽  
Vol 198 ◽  
pp. 37-58 ◽  
Author(s):  
Liping Bai ◽  
Takashi Fujishiro ◽  
Gangfeng Huang ◽  
Jürgen Koch ◽  
Atsushi Takabayashi ◽  
...  

The greenhouse gas and energy carrier methane is produced on Earth mainly by methanogenic archaea. In the hydrogenotrophic methanogenic pathway the reduction of one CO2 to one methane molecule requires four molecules of H2 containing eight electrons. Four of the electrons from two H2 are supplied for reduction of an electron carrier F420, which is catalyzed by F420-reducing [NiFe]-hydrogenase under nickel-sufficient conditions. The same reaction is catalysed under nickel-limiting conditions by [Fe]-hydrogenase coupled with a reaction catalyzed by F420-dependent methylene tetrahydromethanopterin dehydrogenase. [Fe]-hydrogenase contains an iron-guanylylpyridinol (FeGP) cofactor for H2 activation at the active site. FeII of FeGP is coordinated to a pyridinol-nitrogen, an acyl-carbon, two CO and a cysteine-thiolate. We report here on comparative genomic analyses of biosynthetic genes of the FeGP cofactor, which are primarily located in a hmd-co-occurring (hcg) gene cluster. One of the gene products is HcgB which transfers the guanosine monophosphate (GMP) moiety from guanosine triphosphate (GTP) to a pyridinol precursor. Crystal structure analysis of HcgB from Methanococcus maripaludis and its complex with 6-carboxymethyl-3,5-dimethyl-4-hydroxy-2-pyridinol confirmed the physiological guanylyltransferase reaction. Furthermore, we tested the properties of semi-synthetic [Fe]-hydrogenases using the [Fe]-hydrogenase apoenzyme from several methanogenic archaea and a mimic of the FeGP cofactor. On the basis of the enzymatic reactions involved in the methanogenic pathway, we came up with an idea how the methanogenic pathway could be simplified to develop an artificial methanogenesis system.


Author(s):  
Yohei Koizumi ◽  
Masayuki Kuzuhara ◽  
Masashi Omiya ◽  
Teruyuki Hirano ◽  
John Wisniewski ◽  
...  

Abstract We present the optical spectra of 338 nearby M dwarfs, and compute their spectral types, effective temperatures (Teff), and radii. Our spectra were obtained using several optical spectrometers with spectral resolutions that range from 1200 to 10000. As many as 97% of the observed M-type dwarfs have a spectral type of M3–M6, with a typical error of 0.4 subtype, among which the spectral types M4–M5 are the most common. We infer the Teff of our sample by fitting our spectra with theoretical spectra from the PHOENIX model. Our inferred Teff is calibrated with the optical spectra of M dwarfs whose Teff have been well determined with the calibrations that are supported by previous interferometric observations. Our fitting procedures utilize the VO absorption band (7320–7570 Å) and the optical region (5000–8000 Å), yielding typical errors of 128 K (VO band) and 85 K (optical region). We also determine the radii of our sample from their spectral energy distributions. We find most of our sample stars have radii of &lt;0.6 R⊙, with the average error being 3%. Our catalog enables efficient sample selection for exoplanet surveys around nearby M-type dwarfs.


Pathogens ◽  
2021 ◽  
Vol 10 (3) ◽  
pp. 286
Author(s):  
Mary Frances Nakamya ◽  
Moses B. Ayoola ◽  
Leslie A. Shack ◽  
Mirghani Mohamed ◽  
Edwin Swiatlo ◽  
...  

Polyamines such as putrescine, cadaverine, and spermidine are small cationic molecules that play significant roles in cellular processes, including bacterial stress responses and host–pathogen interactions. Streptococcus pneumoniae is an opportunistic human pathogen, which causes several diseases that account for significant morbidity and mortality worldwide. As it transits through different host niches, S. pneumoniae is exposed to and must adapt to different types of stress in the host microenvironment. We earlier reported that S. pneumoniae TIGR4, which harbors an isogenic deletion of an arginine decarboxylase (ΔspeA), an enzyme that catalyzes the synthesis of agmatine in the polyamine synthesis pathway, has a reduced capsule. Here, we report the impact of arginine decarboxylase deletion on pneumococcal stress responses. Our results show that ΔspeA is more susceptible to oxidative, nitrosative, and acid stress compared to the wild-type strain. Gene expression analysis by qRT-PCR indicates that thiol peroxidase, a scavenger of reactive oxygen species and aguA from the arginine deiminase system, could be important for peroxide stress responses in a polyamine-dependent manner. Our results also show that speA is essential for endogenous hydrogen peroxide and glutathione production in S. pneumoniae. Taken together, our findings demonstrate the critical role of arginine decarboxylase in pneumococcal stress responses that could impact adaptation and survival in the host.


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