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(A) Schematic showing the spatial N2O concentration for two inter-cell distances of d = 0 µm (attached) and d = 2 µm (free living). The relative surface N2O concentration for the producer is set to 1, while the relative surface N2O concentration of the consumer is set to 0. The radius of the producer, the radius of the consumer, and the distance between the cells are varied according to the values in Table S2. (B) Volume-normalized uptake rate of N2O for the consumer at 0 µm separation (attached) and 2 µm separation (free living) for all values of the consumer and producer cell sizes. Numbers indicate the actual volume-normalized uptake rates (multiplied by 10⁻¹²). (C) Uptake rates as a function of the inter-cell distance normalized to the attached scenario of the same consumer-producer cell size combination. A value of, e.g., 0.2 indicates that this combination of producer and consumer cell size shows a reduction of 80% in the consumer N2O uptake rate at this distance compared to if they were attached. The spread within a given inter-cell distance is a result of varying the producer and consumer cell sizes (cross-combining five consumer with four producer sizes as shown in panel B). n = 20 simulations plotted for each bar, with box representing ±1 s.d. and the whiskers showing ±2 s.d.
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Archaea belonging to the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have been found in an expanding number of environments and perform a variety of biogeochemical roles, including contributing to carbon, sulfur, and nitrogen cycling. Generally characterized by ultrasmall cell sizes and r...
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Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is currently focused on the bacterial community, while archaea often remain at the sidelines of metaorganism-related research. Here, we describe the archaeome of a total of eleven cla...
Citations
... [12][13][14] The functional role of DPANN archaea in the biosphere remains largely enigmatic. 15,16 Are they friends or foes in natural environments, and do they play an important and cohesive role in microbial consortia that decompose waste? Here, we take a closer look at a three-membered, extremely halophilic natural consortium consisting of the xylan-degrading Halorhabdus sp. ...
... Detailed methods are provided in the online version of this paper and include the following: The model microorganisms used in this study were halophilic archaea isolated from a natural xylan-degrading consortium, [12][13][14][15][16][17]21 consisting of the xylan-degrading Halorhabdus sp. SVX81, the xylose-consuming H. volcanii SVX82 and its ectosymbiont Ca. ...
This study examines a natural consortium of halophilic archaea, comprising xylan-degrading Halorhabdus sp. SVX81, consortium cohabitant Haloferax volcanii SVX82 (formerly H. lucentense SVX82), and its DPANN ectosymbiont Ca. Nanohalococcus occultus SVXNc. Transcriptomics and targeted metabolomics demonstrated that the tripartite consortium outperformed individual and the Halorhabdus sp. SVX81 with H. volcanii SVX82 bipartite cultures in xylan degradation, exhibiting a division of labor: the DPANN symbiont processed glycolysis products, while other members performed xylan depolymerization and biosynthesis of essential compounds. Electron microscopy and cryo-electron tomography revealed the formation of heterocellular biofilms interlinked by DPANN cells. The findings demonstrated that DPANN symbionts can interact directly with other members of microbial communities, which are not their primary hosts, influencing their gene expression. However, DPANN proliferation requires their primary host presence. The study highlights the collective contribution of consortium members to xylan degradation and their potential for biotechnological applications in the management of hypersaline environments.
... A new study by Zhang et al. (11) examined the genomic diversity of DPANN archaea in pelagic oxygen deficient zones (ODZs) from the Arabian Sea and the eastern tropical North and South Pacific regions (ETNP and ETSP). From a set of 962 metagenome assembled genomes (MAGs), they identified 33 belonging to the DPANN phyla Nanoarchaeota, Pacearchaeota, Woesearchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190. ...
... A phylogeny of these DPANN NosZ-like proteins revealed that they are distinct from homologous cytochrome c oxidase subunit II and clade II Sec-type NosZ. Zhang et al. (11) attempted to heterologously express three of the DPANN nosZ-like genes in Pseudomonas aeruginosa. They were unable to confirm any significant N 2 O reduction in the mutants compared to the P. aeruginosa native nosZ complementation. ...
... As N 2 O is present at low nanomolar concentrations in ODZ waters, there may not be enough for any microbes to make a living from its consumption. Zhang et al. (11) explore an alternative scenario where high levels of N 2 O may localize near cells that produce N 2 O such that the characteristically small DPANN may be able to get close enough to these N 2 O producers to survive. In this study, they predict N 2 O reduction feasibility by simulating cell size ratios and distance between cells. ...
DPANN archaea have characteristically small cells and unique genomes that were long overlooked in diversity surveys. Their reduced genomes often lack essential metabolic pathways, requiring symbiotic relationships with other archaeal and bacterial hosts for survival. Yet a long-standing question remains, what is the advantage of maintaining ultrasmall cells. A recent study by Zhang et al. examined genomes of DPANN archaea from marine oxygen deficient zones (ODZs) (I. H. Zhang, B. Borer, R. Zhao, S. Wilbert, et al., mBio 15:e02918-23, 2024, https://doi.org/10.1128/mbio.02918-23). Surprisingly, these genomes contain a broad array of metabolic pathways including genes predicted to be involved in nitrous oxide (N2O) reduction. However, N2O levels are likely too low in ODZs to make this metabolically feasible. Modeling co-localization of DPANN archaea (N2O consumers) with other larger cells (N2O producers) demonstrates that N2O uptake rates can be optimized by maximizing the producer-to-consumer size ratio and proximity of consumer cells to producers. This may explain why such a diversity of archaea maintain extremely small cell sizes.
... These and other "candidatus" cultivations of Nanobdel lati have provided novel insights into their physiology and evolution (10)(11)(12)(13)(14)(15)(16)(17). Despite the extremophilic nature of these currently culturable members, Nanobdellati archaea have also been found in diverse non-extreme environments, including the human oral cavity (18), reflecting their own diversity and their host diversity (5,19,20). Although known Nanobdellati members are obligately ectosymbiotic with specific archaeal strains or species, M. variisymbioticus exhibited a relatively broad host range (9). ...
Members of the kingdom Nanobdellati, previously known as DPANN archaea, are characterized by ultrasmall cell sizes and reduced genomes. They primarily thrive through ectosymbiotic interactions with specific hosts in diverse environments. Recent successful cultivations have emphasized the importance of adhesion to host cells for understanding the ecophysiology of Nanobdellati. Cell adhesion is often mediated by cell surface carbohydrates, and in archaea, this may be facilitated by the glycosylated S-layer protein that typically coats their cell surface. In this study, we conducted glycoproteomic analyses on two co-cultures of Nanobdellati with their host archaea, as well as on pure cultures of both host and non-host archaea. Nanobdellati exhibited various glycoproteins, including archaellins and hypothetical proteins, with glycans that were structurally distinct from those of their hosts. This indicated that Nanobdellati autonomously synthesize their glycans for protein modifications probably using host-derived substrates, despite the high energy cost. Glycan modifications on Nanobdellati proteins consistently occurred on asparagine residues within the N-X-S/T sequon, consistent with patterns observed across archaea, bacteria, and eukaryotes. In both host and non-host archaea, S-layer proteins were commonly modified with hexose, N-acetylhexosamine, and sulfonated deoxyhexose. However, the N-glycan structures of host archaea, characterized by distinct sugars such as deoxyhexose, nonulosonate sugar, and pentose at the nonreducing ends, were implicated in enabling Nanobdellati to differentiate between host and non-host cells. Interestingly, the specific sugar, xylose, was eliminated from the N-glycan in a host archaeon when co-cultured with Nanobdella. These findings enhance our understanding of the role of protein glycosylation in archaeal interactions.
IMPORTANCE
Nanobdellati archaea, formerly known as DPANN, are phylogenetically diverse, widely distributed, and obligately ectosymbiotic. The molecular mechanisms by which Nanobdellati recognize and adhere to their specific hosts remain largely unexplored. Protein glycosylation, a fundamental biological mechanism observed across all domains of life, is often crucial for various cell–cell interactions. This study provides the first insights into the glycoproteome of Nanobdellati and their host and non-host archaea. We discovered that Nanobdellati autonomously synthesize glycans for protein modifications, probably utilizing substrates derived from their hosts. Additionally, we identified distinctive glycosylation patterns that suggest mechanisms through which Nanobdellati differentiate between host and non-host cells. This research significantly advances our understanding of the molecular basis of microbial interactions in extreme environments.
Bacterial membrane lipids are typically characterised by fatty acid bilayers linked through ester bonds, whereas those of Archaea are characterised by ether‐linked isoprenoids forming bilayers or monolayers of membrane‐spanning lipids known as isoprenoidal glycerol dialkyl glycerol tetraethers (isoGDGTs). However, this understanding has been reconsidered with the identification of branched GDGTs (brGDGTs), which are membrane‐spanning ether‐bound branched alkyl fatty acids of bacterial origin, though their producers are often unidentified. The limited availability of microbial cultures constrains the understanding of the biological sources of these membrane lipids, thus limiting their use as biomarkers. To address this issue, we identified membrane lipids in the Black Sea using high‐resolution accurate mass/mass spectrometry and inferred their potential producers by targeting lipid biosynthetic pathways encoded on the metagenome, in metagenome‐assembled genomes and unbinned scaffolds. We also identified brGDGTs and highly branched GDGTs in the suboxic and euxinic waters, potentially attributed to Planctomycetota, Cloacimonadota, Desulfobacterota, Chloroflexota, Actinobacteria and Myxococcota—based on their lipid biosynthetic genomic potential. These findings introduce new possibilities for using specific brGDGTs as biomarkers of anoxic conditions in marine environments and highlight the role of these membrane lipids in microbial adaptation.
Background:
For many years, scientists have accepted Darwin's conclusion that "Survival of the Fittest" involves successful competition with other organisms for life-endowing molecules and conditions.
Summary:
Newly discovered "partial" organisms with minimal genomes that require symbiotic or parasitic relationships for growth and reproduction suggest that cooperation in addition to competition was and still is a primary driving force for survival. These two phenomena are not mutually exclusive, and both can confer a competitive advantage for survival. In fact, cooperation may have been more important in the early evolution for life on Earth before autonomous organisms developed, becoming large genome organisms.
Key messages:
This suggestion has tremendous consequences with respect to our conception of the early evolution of life on Earth as well as the appearance of intercellular interactions, multicellularity and the nature of interactions between humans and their societies (e.g., Social Darwinism).
To explore methods supplementing the insights gained from chemical analysis in understanding landfill conditions, we analyzed the relationship between landfill waste composition, microbial community structure in leachate, and leachate water quality. The principal component analysis of water quality and classification of landfills by waste composition showed that landfills with more plastic had lower total contamination than others. The types of organic and inorganic components in the leachate also varied with the landfill waste composition. The microbial community structure at the phylum level in leachate of inert-waste landfill sites was Proteobacteria emerged as the predominant phylum (55% on average) and Bacteroidetes followed as the second most prevalent (12% on average), while Firmicutes was less dominant (0.3% on average). Additionally, the amount of plastic in the landfill waste was related to cyanobacteria, known for their role in plastic degradation. Microbial taxa involved in organic metabolism and oxidation reactions were related to bicarbonate ion (HCO3‒), and those involved in oxygen-deficient environments and methane fermentation were connected to water quality parameters, such as COD, TOC, EC, inorganic ionic components, and Co. In the future, assessing the proportions of characteristic microbial taxa in leachate could help understand landfill conditions.
Archaea continues to be one of the least investigated domains of life, and in recent years, the advent of metagenomics has led to the discovery of many new lineages at the phylum level. For the majority, only automatic genomic annotations can provide information regarding their metabolic potential and role in the environment. Here, genomic data from 2,978 archaeal genomes was used to perform automatic annotations using bioinformatics tools, alongside synteny analysis. These automatic classifications were done to assess how good these different tools perform in relation to archaeal data. Our study revealed that even with lowered cutoffs, several functional models do not capture the recently discovered archaeal diversity. Moreover, our investigation revealed that a significant portion of archaeal genomes, approximately 42%, remain uncharacterized. In comparison, within 3,235 bacterial genomes, a diverse range of unclassified proteins is obtained, with well-studied organisms like Escherichia coli having a substantially lower proportion of uncharacterized regions, ranging from <5 to 25%, and less studied lineages being comparable to archaea with the range of 35–40% of unclassified regions. Leveraging this analysis, we were able to identify metabolic protein markers, thereby providing insights into the metabolism of the archaea in our dataset. Our findings underscore a substantial gap between automatic classification tools and the comprehensive mapping of archaeal metabolism. Despite advances in computational approaches, a significant portion of archaeal genomes remains unexplored, highlighting the need for extensive experimental validation in this domain, as well as more refined annotation methods. This study contributes to a better understanding of archaeal metabolism and underscores the importance of further research in elucidating the functional potential of archaeal genomes.
Here, I review the dynamic history of prokaryotic phyla. Following leads set by Darwin, Haeckel and Woese, the concept of phylum has evolved from a group sharing common phenotypes to a set of organisms sharing a common ancestry, with modern taxonomy based on phylogenetic classifications drawn from macromolecular sequences. Phyla came as surprising latecomers to the formalities of prokaryotic nomenclature in 2021. Since then names have been validly published for 46 prokaryotic phyla, replacing some established names with neologisms, prompting criticism and debate within the scientific community. Molecular barcoding enabled phylogenetic analysis of microbial ecosystems without cultivation, leading to the identification of candidate divisions (or phyla) from diverse environments. The introduction of metagenome-assembled genomes marked a significant advance in identifying and classifying uncultured microbial phyla. The lumper–splitter dichotomy has led to disagreements, with experts cautioning against the pressure to create a profusion of new phyla and prominent databases adopting a conservative stance. The Candidatus designation has been widely used to provide provisional status to uncultured prokaryotic taxa, with phyla named under this convention now clearly surpassing those with validly published names. The Genome Taxonomy Database (GTDB) has offered a stable, standardized prokaryotic taxonomy with normalized taxonomic ranks, which has led to both lumping and splitting of pre-existing phyla. The GTDB framework introduced unwieldy alphanumeric placeholder labels, prompting recent publication of over 100 user-friendly Latinate names for unnamed prokaryotic phyla. Most candidate phyla remain ‘known unknowns’, with limited knowledge of their genomic diversity, ecological roles, or environments. Whether phyla still reflect significant evolutionary and ecological partitions across prokaryotic life remains an area of active debate. However, phyla remain of practical importance for microbiome analyses, particularly in clinical research. Despite potential diminishing returns in discovery of biodiversity, prokaryotic phyla offer extensive research opportunities for microbiologists for the foreseeable future.
