One highly diverse phylogenetic group of Bacteria,
Ca
. Patescibacteria, remains poorly understood, but, from the few cultured representatives and metagenomic investigations, they are thought to live symbiotically or parasitically with other bacteria or even with eukarya.
The deep ocean microbiota represents the unexplored majority of global ocean waters. The phylum
Chloroflexi
is abundant and broadly distributed in various deep-sea ecosystems.
Manganese (Mn) is an abundant redox-active metal that cycles in many of Earth’s biomes. While diverse bacteria and archaea have been demonstrated to respire Mn(III/IV), only recently have bacteria been implicated in Mn(II) oxidation-dependent growth.
Novymonas esmeraldas
is a parasitic flagellate of the family Trypanosomatidae representing the closest insect-restricted relative of the human pathogen
Leishmania
. It bears symbiotic bacteria in its cytoplasm, the relationship with which has been established relatively recently and independently from other known endosymbioses in protists.
Our results suggest that
Midichloria mitochondrii
, the intramitochondrial bacterium, does not invade mitochondria like predatory bacteria do but instead moves from mitochondrion to mitochondrion within the oocytes of
Ixodes ricinus
. A better understanding of the lifestyle of
M. mitochondrii
will allow us to better define the role of this bacterial symbiont in the host physiology.
In the seabed, gaseous alkanes are oxidized by syntrophic microbial consortia that thereby reduce fluxes of these compounds into the water column. Because of the immense quantities of seabed alkane fluxes, these consortia are key catalysts of the global carbon cycle. Due to their obligate syntrophic lifestyle, the physiology of alkane-degrading archaea remains poorly understood. We have now cultivated a thermophilic, relatively fast-growing ethane oxidizer in partnership with a sulfate-reducing bacterium known to aid in methane oxidation and have retrieved the first complete genome of a short-chain alkane-degrading archaeon. This will greatly enhance the understanding of nonmethane alkane activation by noncanonical methyl-coenzyme M reductase enzymes and provide insights into additional metabolic steps and the mechanisms underlying syntrophic partnerships. Ultimately, this knowledge could lead to the biotechnological development of alkanogenic microorganisms to support the carbon neutrality of industrial processes.
Oil-rich sediments from the Gulf of Mexico were found to contain diverse alkane-degrading groups of archaea. The symbiotic, consortium-forming “
Candidatus
Argoarchaeum” and “
Candidatus
Syntrophoarchaeum” are likely responsible for the degradation of ethane and short-chain alkanes, with the help of sulfate-reducing bacteria. “
Ca.
Methanoliparia” occurs as single cells associated with oil droplets. These archaea encode two phylogenetically different methyl-coenzyme M reductases that may allow this organism to thrive as a methanogen on a substrate of long-chain alkanes. Based on a library survey, we show that “
Ca. Methanoliparia
” is frequently detected in oil reservoirs and may be a key agent in the transformation of long-chain alkanes to methane. Our findings provide evidence for the important and diverse roles of archaea in alkane-rich marine habitats and support the notion of a significant functional versatility of the methyl coenzyme M reductase.
The symbiotic N
2
-fixing cyanobacterium UCYN-A, which is closely related to
Braarudosphaera bigelowii
, and its eukaryotic algal host have been shown to be globally distributed and important in open-ocean N
2
fixation. These unique cyanobacteria have reduced metabolic capabilities, even lacking genes for oxygenic photosynthesis and carbon fixation. Cyanobacteria generally use energy from photosynthesis for nitrogen fixation but require mechanisms for avoiding inactivation of the oxygen-sensitive nitrogenase enzyme by ambient oxygen (O
2
) or the O
2
evolved through photosynthesis. This study showed that symbiosis between the N
2
-fixing cyanobacterium UCYN-A and its eukaryotic algal host has led to adaptation of its daily gene expression pattern in order to enable daytime aerobic N
2
fixation, which is likely more energetically efficient than fixing N
2
at night, as found in other unicellular marine cyanobacteria.
ABSTRACT
Nitrification is a key process of the biogeochemical nitrogen cycle and of biological wastewater treatment. The second step, nitrite oxidation to nitrate, is catalyzed by phylogenetically diverse, chemolithoautotrophic nitrite-oxidizing bacteria (NOB). Uncultured NOB from the genus “
Candidatus
Nitrotoga” are widespread in natural and engineered ecosystems. Knowledge about their biology is sparse, because no genomic information and no pure “
Ca
. Nitrotoga” culture was available. Here we obtained the first “
Ca
. Nitrotoga” isolate from activated sludge. This organism, “
Candidatus
Nitrotoga fabula,” prefers higher temperatures (>20°C; optimum, 24 to 28°C) than previous “
Ca
. Nitrotoga” enrichments, which were described as cold-adapted NOB. “
Ca
. Nitrotoga fabula” also showed an unusually high tolerance to nitrite (activity at 30 mM NO
2
−
) and nitrate (up to 25 mM NO
3
−
). Nitrite oxidation followed Michaelis-Menten kinetics, with an apparent
K
m
(
K
m
(app)
) of ~89 µM nitrite and a
V
max
of ~28 µmol of nitrite per mg of protein per h. Key metabolic pathways of “
Ca
. Nitrotoga fabula” were reconstructed from the closed genome. “
Ca
. Nitrotoga fabula” possesses a new type of periplasmic nitrite oxidoreductase belonging to a lineage of mostly uncharacterized proteins. This novel enzyme indicates (i) separate evolution of nitrite oxidation in “
Ca
. Nitrotoga” and other NOB, (ii) the possible existence of phylogenetically diverse, unrecognized NOB, and (iii) together with new metagenomic data, the potential existence of nitrite-oxidizing archaea. For carbon fixation, “
Ca
. Nitrotoga fabula” uses the Calvin-Benson-Bassham cycle. It also carries genes encoding complete pathways for hydrogen and sulfite oxidation, suggesting that alternative energy metabolisms enable “
Ca
. Nitrotoga fabula” to survive nitrite depletion and colonize new niches.
IMPORTANCE
Nitrite-oxidizing bacteria (NOB) are major players in the biogeochemical nitrogen cycle and critical for wastewater treatment. However, most NOB remain uncultured, and their biology is poorly understood. Here, we obtained the first isolate from the environmentally widespread NOB genus “
Candidatus
Nitrotoga” and performed a detailed physiological and genomic characterization of this organism (“
Candidatus
Nitrotoga fabula”). Differences between key phenotypic properties of “
Ca
. Nitrotoga fabula” and those of previously enriched “
Ca
. Nitrotoga” members reveal an unexpectedly broad range of physiological adaptations in this genus. Moreover, genes encoding components of energy metabolisms outside nitrification suggest that “
Ca
. Nitrotoga” are ecologically more flexible than previously anticipated. The identification of a novel nitrite-oxidizing enzyme in “
Ca
. Nitrotoga fabula” expands our picture of the evolutionary history of nitrification and might lead to discoveries of novel nitrite oxidizers. Altogether, this study provides urgently needed insights into the biology of understudied but environmentally and biotechnologically important microorganisms.