Sulfur-cycling microorganisms impact organic matter decomposition in wetlands and consequently greenhouse gas emissions from these globally relevant environments. However, their identities and physiological properties are largely unknown. By applying a functional metagenomics approach to an acidic peatland, we recovered draft genomes of seven novel Acidobacteria species with the potential for dissimilatory sulfite (dsrAB, dsrC, dsrD, dsrN, dsrT, dsrMKJOP) or sulfate respiration (sat, aprBA, qmoABC plus dsr genes). Surprisingly, the genomes also encoded DsrL, which so far was only found in sulfur-oxidizing microorganisms. Metatranscriptome analysis demonstrated expression of acidobacterial sulfur-metabolism genes in native peat soil and their upregulation in diverse anoxic microcosms. This indicated an active sulfate respiration pathway, which, however, might also operate in reverse for dissimilatory sulfur oxidation or disproportionation as proposed for the sulfur-oxidizing Desulfurivibrio alkaliphilus. Acidobacteria that only harbored genes for sulfite reduction additionally encoded enzymes that liberate sulfite from organosulfonates, which suggested organic sulfur compounds as complementary energy sources. Further metabolic potentials included polysaccharide hydrolysis and sugar utilization, aerobic respiration, several fermentative capabilities, and hydrogen oxidation. Our findings extend both, the known physiological and genetic properties of Acidobacteria and the known taxonomic diversity of microorganisms with a DsrAB-based sulfur metabolism, and highlight new fundamental niches for facultative anaerobic Acidobacteria in wetlands based on exploitation of inorganic and organic sulfur molecules for energy conservation.
Chlamydiae have been known for more than a century as major pathogens of humans. Yet they are also found ubiquitously in the environment where they thrive within protists and in an unmatched wide range of animals. This review summarizes recent advances in understanding chlamydial diversity and distribution in nature. Studying these environmental chlamydiae provides a novel perspective on basic chlamydial biology and evolution. A picture is beginning to emerge with chlamydiae representing one of the evolutionarily most ancient and successful groups of obligate intracellular bacteria. A Chlamydia for Every EukaryoteChlamydiae are a major cause of eye infections (trachoma) and sexually transmitted disease, being responsible for an estimated 2 million and 130 million infections worldwide per year, respectively [1]. They were originally described as a small, well-separated group of bacteria infecting humans and birds through an unusual and strictly intracellular developmental cycle. During the past two decades, novel chlamydiae have been discovered within protists such as amoebae, and in diverse animal hosts [2,3]. Interchangeably referred to as chlamydia-like organisms (CLOs) or environmental chlamydiae (see Glossary), studying these environmental microbes revealed striking similarities with, and unexpected differences to, the wellknown human pathogens Chlamydia trachomatis, C. pneumoniae, and C.psittaci [2][3][4].A number of review articles have addressed the discovery of these novel chlamydiae, selected aspects of their biology, their interaction with hosts, and their potential role as human and animal pathogens [2][3][4][5][6][7][8][9][10][11][12][13][14]. Here, we focus on accumulating evidence for a widespread occurrence of chlamydiae in diverse environments, as members of various microbiomes, and in a wide range of hoststogether indicating that chlamydiae are indeed ubiquitous in nature. Following the paradigm that (chlamydial) pathogens once originated from environmental bacteria, we highlight recent environmental chlamydia research about fundamental aspects of chlamydial biology, and we show how studying these environmental representatives provides a framework for understanding the evolution of this unique group of intracellular microbes. Microbiome Research Recovers Novel ChlamydiaeOwing to their obligate intracellular lifestyle, chlamydiae are inherently difficult to study and their retrieval directly from environmental samples is challenging. The application of next-generation sequencing techniques in amplicon, single-cell, and metagenome studies has thus been instrumental in investigating chlamydial diversity and biology [15]. Recent technological advances enabled deep sampling as well as deep sequencing, facilitating the recovery of rare taxa in diverse microbiomes and environments. This revealed a hitherto underestimated broad distribution of chlamydiae in nature and a surprisingly high abundance in some habitats [10,[16][17][18][19][20][21][22]. Diversity of Chlamydiae in the EnvironmentRepresentatives...
Chlamydiae are highly successful strictly intracellular bacteria associated with diverse eukaryotic hosts. Here we analyzed metagenome-assembled genomes of the “Genomes from Earth’s Microbiomes” initiative from diverse environmental samples, which almost double the known phylogenetic diversity of the phylum and facilitate a highly resolved view at the chlamydial pangenome. Chlamydiae are defined by a relatively large core genome indicative of an intracellular lifestyle, and a highly dynamic accessory genome of environmental lineages. We observe chlamydial lineages that encode enzymes of the reductive tricarboxylic acid cycle and for light-driven ATP synthesis. We show a widespread potential for anaerobic energy generation through pyruvate fermentation or the arginine deiminase pathway, and we add lineages capable of molecular hydrogen production. Genome-informed analysis of environmental distribution revealed lineage-specific niches and a high abundance of chlamydiae in some habitats. Together, our data provide an extended perspective of the variability of chlamydial biology and the ecology of this phylum of intracellular microbes.
The evolution of obligate host-association of bacterial symbionts and pathogens remains poorly understood. The Rickettsiales are an alphaproteobacterial order of obligate endosymbionts and parasites that infect a wide variety of eukaryotic hosts, including humans, livestock, insects and protists. Induced by their host-associated lifestyle, Rickettsiales genomes have undergone reductive evolution, leading to small, AT-rich genomes with limited metabolic capacities. Here we uncover eleven deep-branching alphaproteobacterial metagenome assembled genomes from aquatic environments, including data from the Tara Oceans initiative and other publicly available datasets, distributed over three previously undescribed Rickettsiales-related clades. Phylogenomic analyses reveal that two of these clades, Mitibacteraceae and Athabascaceae, branch sister to all previously sampled Rickettsiales. The third clade, Gamibacteraceae, branch sister to the recently identified ectosymbiotic ‘Candidatus Deianiraea vastatrix’. Comparative analyses indicate that the gene complement of Mitibacteraceae and Athabascaceae is reminiscent of that of free-living and biofilm-associated bacteria. Ancestral genome content reconstruction across the Rickettsiales species tree further suggests that the evolution of host association in Rickettsiales was a gradual process that may have involved the repurposing of a type IV secretion system.
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