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Article ; Online: An abundant bacterial phylum with nitrite-oxidizing potential in oligotrophic marine sediments.

Zhao, Rui / Jørgensen, Steffen L / Babbin, Andrew R

Communications biology

2024 Volume 7, Issue 1, Page(s) 449

Abstract: Nitrite-oxidizing bacteria (NOB) are important nitrifiers whose activity regulates the availability of nitrite and dictates the magnitude of nitrogen loss in ecosystems. In oxic marine sediments, ammonia-oxidizing archaea (AOA) and NOB together catalyze ... ...

Abstract	Nitrite-oxidizing bacteria (NOB) are important nitrifiers whose activity regulates the availability of nitrite and dictates the magnitude of nitrogen loss in ecosystems. In oxic marine sediments, ammonia-oxidizing archaea (AOA) and NOB together catalyze the oxidation of ammonium to nitrate, but the abundance ratios of AOA to canonical NOB in some cores are significantly higher than the theoretical ratio range predicted from physiological traits of AOA and NOB characterized under realistic ocean conditions, indicating that some NOBs are yet to be discovered. Here we report a bacterial phylum Candidatus Nitrosediminicolota, members of which are more abundant than canonical NOBs and are widespread across global oligotrophic sediments. Ca. Nitrosediminicolota members have the functional potential to oxidize nitrite, in addition to other accessory functions such as urea hydrolysis and thiosulfate reduction. While one recovered species (Ca. Nitrosediminicola aerophilus) is generally confined within the oxic zone, another (Ca. Nitrosediminicola anaerotolerans) additionally appears in anoxic sediments. Counting Ca. Nitrosediminicolota as a nitrite-oxidizer helps to resolve the apparent abundance imbalance between AOA and NOB in oxic marine sediments, and thus its activity may exert controls on the nitrite budget.
MeSH term(s)	Nitrites ; Ecosystem ; Bacteria/genetics ; Oxidation-Reduction ; Geologic Sediments/microbiology
Chemical Substances	Nitrites
Language	English
Publishing date	2024-04-11
Publishing country	England
Document type	Journal Article
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-024-06136-2
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen-deficient zones with diverse metabolic potential.

Zhang, Irene H / Borer, Benedict / Zhao, Rui / Wilbert, Steven / Newman, Dianne K / Babbin, Andrew R

mBio

2024 Volume 15, Issue 3, Page(s) e0291823

Abstract: 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 ...

Abstract	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 reduced genomes, DPANN archaea may form mutualistic, commensal, or parasitic interactions with various archaeal and bacterial hosts, influencing the ecology and functioning of microbial communities. While DPANN archaea reportedly comprise a sizeable fraction of the archaeal community within marine oxygen-deficient zone (ODZ) water columns, little is known about their metabolic capabilities in these ecosystems. We report 33 novel metagenome-assembled genomes (MAGs) belonging to the DPANN phyla Nanoarchaeota, Pacearchaeota, Woesearchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190 from pelagic ODZs in the Eastern Tropical North Pacific and the Arabian Sea. We find these archaea to be permanent, stable residents of all three major ODZs only within anoxic depths, comprising up to 1% of the total microbial community and up to 25%-50% of archaea as estimated from read mapping to MAGs. ODZ DPANN appear to be capable of diverse metabolic functions, including fermentation, organic carbon scavenging, and the cycling of sulfur, hydrogen, and methane. Within a majority of ODZ DPANN, we identify a gene homologous to nitrous oxide reductase. Modeling analyses indicate the feasibility of a nitrous oxide reduction metabolism for host-attached symbionts, and the small genome sizes and reduced metabolic capabilities of most DPANN MAGs suggest host-associated lifestyles within ODZs. Importance: Archaea from the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have diverse metabolic capabilities and participate in multiple biogeochemical cycles. While metagenomics and enrichments have revealed that many DPANN are characterized by ultrasmall genomes, few biosynthetic genes, and episymbiotic lifestyles, much remains unknown about their biology. We report 33 new DPANN metagenome-assembled genomes originating from the three global marine oxygen-deficient zones (ODZs), the first from these regions. We survey DPANN abundance and distribution within the ODZ water column, investigate their biosynthetic capabilities, and report potential roles in the cycling of organic carbon, methane, and nitrogen. We test the hypothesis that nitrous oxide reductases found within several ODZ DPANN genomes may enable ultrasmall episymbionts to serve as nitrous oxide consumers when attached to a host nitrous oxide producer. Our results indicate DPANN archaea as ubiquitous residents within the anoxic core of ODZs with the potential to produce or consume key compounds.
MeSH term(s)	Archaea/genetics ; Nitrous Oxide/metabolism ; Phylogeny ; Metagenome ; Microbiota ; Methane/metabolism ; Oxygen/metabolism ; Carbon/metabolism ; Nitrogen/metabolism ; Sulfur/metabolism ; Water/metabolism
Chemical Substances	Nitrous Oxide (K50XQU1029) ; Methane (OP0UW79H66) ; Oxygen (S88TT14065) ; Carbon (7440-44-0) ; Nitrogen (N762921K75) ; Sulfur (70FD1KFU70) ; Water (059QF0KO0R)
Language	English
Publishing date	2024-02-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mbio.02918-23
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Microscale advection governs microbial growth and oxygen consumption in macroporous aggregates.

Shen, Rachel / Borer, Benedict / Ciccarese, Davide / Salek, M Mehdi / Babbin, Andrew R

mSphere

2024 Volume 9, Issue 4, Page(s) e0018524

Abstract: Most microbial life on Earth is found in localized microenvironments that collectively exert a crucial role in maintaining ecosystem health and influencing global biogeochemical cycles. In many habitats such as biofilms in aquatic systems, bacterial ... ...

Abstract	Most microbial life on Earth is found in localized microenvironments that collectively exert a crucial role in maintaining ecosystem health and influencing global biogeochemical cycles. In many habitats such as biofilms in aquatic systems, bacterial flocs in activated sludge, periphyton mats, or particles sinking in the ocean, these microenvironments experience sporadic or continuous flow. Depending on their microscale structure, pores and channels through the microenvironments permit localized flow that shifts the relative importance of diffusive and advective mass transport. How this flow alters nutrient supply, facilitates waste removal, drives the emergence of different microbial niches, and impacts the overall function of the microenvironments remains unclear. Here, we quantify how pores through microenvironments that permit flow can elevate nutrient supply to the resident bacterial community using a microfluidic experimental system and gain further insights from coupled population-based and computational fluid dynamics simulations. We find that the microscale structure determines the relative contribution of advection vs diffusion, and even a modest flow through a pore in the range of 10 µm s
Language	English
Publishing date	2024-03-26
Publishing country	United States
Document type	Journal Article
ISSN	2379-5042
ISSN (online)	2379-5042
DOI	10.1128/msphere.00185-24
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Article ; Online: Age, metabolisms, and potential origin of dominant anammox bacteria in the global oxygen-deficient zones.

Zhao, Rui / Zhang, Irene H / Jayakumar, Amal / Ward, Bess B / Babbin, Andrew R

ISME communications

2024 Volume 4, Issue 1, Page(s) ycae060

Abstract: Anammox bacteria inhabiting oxygen-deficient zones (ODZs) are a major functional group mediating fixed nitrogen loss in the global ocean. However, many basic questions regarding the diversity, broad metabolisms, origin, and adaptive mechanisms of ODZ ... ...

Abstract	Anammox bacteria inhabiting oxygen-deficient zones (ODZs) are a major functional group mediating fixed nitrogen loss in the global ocean. However, many basic questions regarding the diversity, broad metabolisms, origin, and adaptive mechanisms of ODZ anammox bacteria remain unaddressed. Here we report two novel metagenome-assembled genomes of anammox bacteria affiliated with the
Language	English
Publishing date	2024-04-22
Publishing country	England
Document type	Journal Article
ISSN	2730-6151
ISSN (online)	2730-6151
DOI	10.1093/ismeco/ycae060
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Article ; Online: "

Zhao, Rui / Le Moine Bauer, Sven / Babbin, Andrew R

Applied and environmental microbiology

2023 Volume 89, Issue 8, Page(s) e0080023

Abstract: Bacteria specialized in anaerobic ammonium oxidation (anammox) are widespread in many anoxic habitats and form an important functional guild in the global nitrogen cycle by consuming bio-available nitrogen for energy rather than biomass production. Due ... ...

Abstract	Bacteria specialized in anaerobic ammonium oxidation (anammox) are widespread in many anoxic habitats and form an important functional guild in the global nitrogen cycle by consuming bio-available nitrogen for energy rather than biomass production. Due to their slow growth rates, cultivation-independent approaches have been used to decipher their diversity across environments. However, their full diversity has not been well recognized. Here, we report a new family of putative anammox bacteria, "
MeSH term(s)	Humans ; Nitrites/metabolism ; Nitrates/metabolism ; Anaerobic Ammonia Oxidation ; Phylogeny ; Geologic Sediments/microbiology ; Bacteria ; Ammonium Compounds/metabolism ; Oxidoreductases/metabolism ; Nitrite Reductases/genetics ; Oxidation-Reduction ; Nitrogen/metabolism ; Anaerobiosis ; RNA, Ribosomal, 16S/genetics
Chemical Substances	Nitrites ; Nitrates ; Ammonium Compounds ; Oxidoreductases (EC 1.-) ; Nitrite Reductases (EC 1.7.-) ; Nitrogen (N762921K75) ; RNA, Ribosomal, 16S
Language	English
Publishing date	2023-07-20
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	223011-2
ISSN	1098-5336 ; 0099-2240
ISSN (online)	1098-5336
ISSN	0099-2240
DOI	10.1128/aem.00800-23
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Denitrifying bacteria respond to and shape microscale gradients within particulate matrices.

Smriga, Steven / Ciccarese, Davide / Babbin, Andrew R

Communications biology

2021 Volume 4, Issue 1, Page(s) 570

Abstract: Heterotrophic denitrification enables facultative anaerobes to continue growing even when limited by oxygen ( ... ...

Abstract	Heterotrophic denitrification enables facultative anaerobes to continue growing even when limited by oxygen (O
MeSH term(s)	Bacteria/growth & development ; Bacteria/metabolism ; Denitrification ; Nitrate Reductase/metabolism ; Nitrite Reductases/metabolism ; Nitrogen/metabolism ; Oxygen/metabolism
Chemical Substances	Nitrite Reductases (EC 1.7.-) ; Nitrate Reductase (EC 1.7.99.4) ; Nitrogen (N762921K75) ; Oxygen (S88TT14065)
Language	English
Publishing date	2021-05-13
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-021-02102-4
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Article ; Online: Partitioning of the denitrification pathway and other nitrite metabolisms within global oxygen deficient zones.

Zhang, Irene H / Sun, Xin / Jayakumar, Amal / Fortin, Samantha G / Ward, Bess B / Babbin, Andrew R

ISME communications

2023 Volume 3, Issue 1, Page(s) 76

Abstract: Oxygen deficient zones (ODZs) account for about 30% of total oceanic fixed nitrogen loss via processes including denitrification, a microbially mediated pathway proceeding stepwise from ... ...

Abstract	Oxygen deficient zones (ODZs) account for about 30% of total oceanic fixed nitrogen loss via processes including denitrification, a microbially mediated pathway proceeding stepwise from NO
Language	English
Publishing date	2023-07-20
Publishing country	England
Document type	Journal Article
ISSN	2730-6151
ISSN (online)	2730-6151
DOI	10.1038/s43705-023-00284-y
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Nitrite accumulation and anammox bacterial niche partitioning in Arctic Mid-Ocean Ridge sediments.

Zhao, Rui / Babbin, Andrew R / Roerdink, Desiree L / Thorseth, Ingunn H / Jørgensen, Steffen L

ISME communications

2023 Volume 3, Issue 1, Page(s) 26

Abstract: By consuming ammonium and nitrite, anammox bacteria form an important functional guild in nitrogen cycling in many environments, including marine sediments. However, their distribution and impact on the important substrate nitrite has not been well ... ...

Abstract	By consuming ammonium and nitrite, anammox bacteria form an important functional guild in nitrogen cycling in many environments, including marine sediments. However, their distribution and impact on the important substrate nitrite has not been well characterized. Here we combined biogeochemical, microbiological, and genomic approaches to study anammox bacteria and other nitrogen cycling groups in two sediment cores retrieved from the Arctic Mid-Ocean Ridge (AMOR). We observed nitrite accumulation in these cores, a phenomenon also recorded at 28 other marine sediment sites and in analogous aquatic environments. The nitrite maximum coincides with reduced abundance of anammox bacteria. Anammox bacterial abundances were at least one order of magnitude higher than those of nitrite reducers and the anammox abundance maxima were detected in the layers above and below the nitrite maximum. Nitrite accumulation in the two AMOR cores co-occurs with a niche partitioning between two anammox bacterial families (Candidatus Bathyanammoxibiaceae and Candidatus Scalinduaceae), likely dependent on ammonium availability. Through reconstructing and comparing the dominant anammox genomes (Ca. Bathyanammoxibius amoris and Ca. Scalindua sediminis), we revealed that Ca. B. amoris has fewer high-affinity ammonium transporters than Ca. S. sediminis and lacks the capacity to access alternative substrates and/or energy sources such as urea and cyanate. These features may restrict Ca. Bathyanammoxibiaceae to conditions of higher ammonium concentrations. These findings improve our understanding about nitrogen cycling in marine sediments by revealing coincident nitrite accumulation and niche partitioning of anammox bacteria.
Language	English
Publishing date	2023-03-29
Publishing country	England
Document type	Journal Article
ISSN	2730-6151
ISSN (online)	2730-6151
DOI	10.1038/s43705-023-00230-y
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen deficient zones with diverse metabolic potential.

Zhang, Irene H / Borer, Benedict / Zhao, Rui / Wilbert, Steven / Newman, Dianne K / Babbin, Andrew R

bioRxiv : the preprint server for biology

2023

Abstract: Archaea belonging to the DPANN superphylum have been found within an expanding number of environments and perform a variety of biogeochemical roles, including contributing to carbon, sulfur, and nitrogen cycling. Generally characterized by ultrasmall ... ...

Abstract	Archaea belonging to the DPANN superphylum have been found within 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 reduced genomes, DPANN archaea may form mutualistic, commensal, or parasitic interactions with various archaeal and bacterial hosts, influencing the ecology and functioning of microbial communities. While DPANN archaea reportedly comprise 15-26% of the archaeal community within marine oxygen deficient zone (ODZ) water columns, little is known about their metabolic capabilities in these ecosystems. We report 33 novel metagenome-assembled genomes belonging to DPANN phyla Nanoarchaeota, Pacearchaeota, Woesarchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190 from pelagic ODZs in the Eastern Tropical North Pacific and Arabian Sea. We find these archaea to be permanent, stable residents of all 3 major ODZs only within anoxic depths, comprising up to 1% of the total microbial community and up to 25-50% of archaea. ODZ DPANN appear capable of diverse metabolic functions, including fermentation, organic carbon scavenging, and the cycling of sulfur, hydrogen, and methane. Within a majority of ODZ DPANN, we identify a gene homologous to nitrous oxide reductase. Modeling analyses indicate the feasibility of a nitrous oxide reduction metabolism for host-attached symbionts, and the small genome sizes and reduced metabolic capabilities of most DPANN MAGs suggest host-associated lifestyles within ODZs.
Language	English
Publishing date	2023-10-30
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.10.30.564641
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Article ; Online: Microscale dynamics promote segregated denitrification in diatom aggregates sinking slowly in bulk oxygenated seawater.

Ciccarese, Davide / Tantawi, Omar / Zhang, Irene H / Plata, Desiree / Babbin, Andrew R

Communications earth & environment

2023 Volume 4, Issue 1, Page(s) 275

Abstract: Sinking marine particles drive the biological pump that naturally sequesters carbon from the atmosphere. Despite their small size, the compartmentalized nature of particles promotes intense localized metabolic activity by their bacterial colonizers. Yet ... ...

Abstract	Sinking marine particles drive the biological pump that naturally sequesters carbon from the atmosphere. Despite their small size, the compartmentalized nature of particles promotes intense localized metabolic activity by their bacterial colonizers. Yet the mechanisms promoting the onset of denitrification, a metabolism that arises once oxygen is limiting, remain to be established. Here we show experimentally that slow sinking aggregates composed of marine diatoms-important primary producers for global carbon export-support active denitrification even among bulk oxygenated water typically thought to exclude anaerobic metabolisms. Denitrification occurs at anoxic microsites distributed throughout a particle and within microns of a particle's boundary, and fluorescence-reporting bacteria show nitrite can be released into the water column due to segregated dissimilatory reduction of nitrate and nitrite. Examining intact and broken diatoms as organic sources, we show slowly leaking cells promote more bacterial growth, allow particles to have lower oxygen, and generally support greater denitrification.
Language	English
Publishing date	2023-07-28
Publishing country	England
Document type	Journal Article
ISSN	2662-4435
ISSN (online)	2662-4435
DOI	10.1038/s43247-023-00935-x
Database	MEDical Literature Analysis and Retrieval System OnLINE

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