ABSTRACT
The phylum
Gemmatimonadota
comprises mainly uncultured microorganisms that inhabit different environments such as soils, freshwater lakes, marine sediments, sponges, or corals. Based on 16S rRNA gene studies, the group PAUC43f is one of the most frequently retrieved
Gemmatimonadota
in marine samples. However, its physiology and ecological roles are completely unknown since, to date, not a single PAUC43f isolate or metagenome-assembled genome (MAG) has been characterized. Here, we carried out a broad study of the distribution, abundance, ecotaxonomy, and metabolism of PAUC43f, for which we propose the name of
Palauibacterales
. This group was detected in 4,965 16S rRNA gene amplicon datasets, mainly from marine sediments, sponges, corals, soils, and lakes, reaching up to 34.3% relative abundance, which highlights its cosmopolitan character, mainly salt-related. The potential metabolic capabilities inferred from 52
Palauibacterales
MAGs recovered from marine sediments, sponges, and saline soils suggested a facultative aerobic and chemoorganotrophic metabolism, although some members may also oxidize hydrogen. Some
Palauibacterales
species might also play an environmental role as N
2
O consumers as well as suppliers of serine and thiamine. When compared to the rest of the
Gemmatimonadota
phylum, the biosynthesis of thiamine was one of the key features of the
Palauibacterales
. Finally, we show that polysaccharide utilization loci (PUL) are widely distributed within the
Gemmatimonadota
so that they are not restricted to
Bacteroidetes
, as previously thought. Our results expand the knowledge about this cryptic phylum and provide new insights into the ecological roles of the
Gemmatimonadota
in the environment.
IMPORTANCE
Despite advances in molecular and sequencing techniques, there is still a plethora of unknown microorganisms with a relevant ecological role. In the last years, the mostly uncultured
Gemmatimonadota
phylum is attracting scientific interest because of its widespread distribution and abundance, but very little is known about its ecological role in the marine ecosystem. Here we analyze the global distribution and potential metabolism of the marine
Gemmatimonadota
group PAUC43f, for which we propose the name of
Palauibacterales
order. This group presents a saline-related character and a chemoorganoheterotrophic and facultatively aerobic metabolism, although some species might oxidize H
2
. Given that
Palauibacterales
is potentially able to synthesize thiamine, whose auxotrophy is the second most common in the marine environment, we propose
Palauibacterales
as a key thiamine supplier to the marine communities. This finding suggests that
Gemmatimonadota
could have a more relevant role in the marine environment than previously thought.
“
Candidatus
Parvarchaeales” microbes may represent a lineage uniquely distributed in extreme environments such as AMD and hot springs. However, little is known about the strategies and processes of how they adapted to these extreme environments.
The DPANN superphylum is a group of archaea widely distributed in various habitats. They generally have small cells and have a symbiotic lifestyle with other archaea.
“CandidatusAccumulibacter” is the most studied PAO, with a primary role in biological nutrient removal. However, the species-level taxonomy of this lineage is convoluted due to the use of different phylogenetic markers or genome sequencing approaches. Here, we redefined the phylogeny of these organisms, proposing a comprehensive approach which could be used to address the classification of other diverse and uncultivated lineages.
Recent advances in sequencing technology promoted the blowout discovery of super tiny microbes in the
Diapherotrites
,
Parvarchaeota
,
Aenigmarchaeota
,
Nanoarchaeota
, and
Nanohaloarchaeota
(DPANN) superphylum. However, the unculturable properties of the majority of microbes impeded our investigation of their behavior and symbiotic lifestyle in the corresponding community.
Ammonia tolerance of AOA is usually much lower than that of the AOB, which makes the AOB rather than AOA a predominant ammonia oxidizer in agricultural soils, contributing to global N
2
O emission. Recently, some AOA species from the genus “
Ca.
Nitrosocosmicus” were also found to have high ammonia tolerance.
Microbiology is in a new age in which sequence databases are primary sources of information about many microbes. However, in-depth analysis of environmental genomes thus retrieved is essential to substantiate the new knowledge.
“
Candidatus
Accumulibacter phosphatis” is widely found in full-scale wastewater treatment plants, where it has been identified as the key organism for biological removal of phosphorus. Since aeration can account for 50% of the energy use during wastewater treatment, microaerobic conditions for wastewater treatment have emerged as a cost-effective alternative to conventional biological nutrient removal processes. Our report provides strong genomics-based evidence not only that “
Ca
. Accumulibacter phosphatis” is the main organism contributing to phosphorus removal under microaerobic conditions but also that this organism simultaneously respires nitrate and oxygen in this environment, consequently removing nitrogen and phosphorus from the wastewater. Such activity could be harnessed in innovative designs for cost-effective and energy-efficient optimization of wastewater treatment systems.
Secondary metabolites, which are small-molecule organic compounds produced by living organisms, provide or inspire drugs for many different diseases. These natural products have evolved over millions of years to provide a survival benefit to the producing organism and often display potent biological activity with important therapeutic applications. For instance, defensive compounds in the environment may be cytotoxic to eukaryotic cells, a property exploitable for cancer treatment. Here, we describe the genome of an uncultured symbiotic bacterium that makes such a cytotoxic metabolite. This symbiont is losing genes that do not endow a selective advantage in a hospitable host environment. Secondary metabolism genes, however, are repeated multiple times in the genome, directly demonstrating their selective advantage. This finding shows the strength of selective forces in symbiotic relationships and suggests that uncultured bacteria in such relationships should be targeted for drug discovery efforts.