Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea

Li, Meng; Baker, Brett J.; Anantharaman, Karthik; Jain, Sunit; Breier, J. A.; Dick, Gregory J.

doi:10.1038/ncomms9933

Cited by 146 publications

(190 citation statements)

References 72 publications

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“…These references recruited 56−95% of all archaeal reads. A separately defined set of MG-II/III genomic bins (Li et al 2015) did not improve this recruitment. All annotations used were based on the original annotations of the 997 published contigs.…”

Section: Bioinformatics Analysis Of Metatranscriptomesmentioning

confidence: 80%

Winter mixing impacts gene expression in marine microbial populations in the Gulf of Aqaba

Miller¹,

Pfreundt²,

Hou³

et al. 2017

Aquat. Microb. Ecol.

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In aquatic systems, changes in temperature and irradiance fundamentally characterize the water column and regulate microbial population structure and function. In systems with stable thermal stratification, the warm surface mixed layer is typically nutrient impoverished, limiting biological production. In periods of destratification, convective mixing of the water column exposes the microorganisms inhabiting these mixed systems to rapid variations in light availability and spectra. We explored the impact of winter deep-mixing (500 m deep mixed layer) on microbial communities from the surface (2.5 m) and the aphotic waters (440 m) in the Gulf of Aqaba by examining changes in both population composition and function via DNA and RNA sequencing. The greatest fraction of 16S sequences was assigned to Euryarchaeota, while metatranscriptomes were dominated by Synechococcus transcripts. Community composition was highly similar at both depths, yet transcription profiles differed. Phototrophic organisms found at the photic surface overexpressed genes related to catabolism and energy metabolism, while genes affiliated with biosynthesis were overexpressed at the aphotic depth. Similar transcriptional trends were observed in the non-photoautotrophs SAR11, Euryarchaeota, and Thaumarchaeota, with niche partitioning based on differential utilization of nitrogen and phosphorus occurring between the 2 archaeal groups. We did not detect upregulated expression of cyanobacterial genes indicative of mixotrophy or glycogen metabolism in the aphotic zone, suggesting they survive the aphotic period by utilizing photosynthates produced in the photic zone. Indications for a mixotrophic lifestyle were observed for prasinophytes, with genes related to phagocytosis overexpressed at the aphotic depth compared with the surface.

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Section: Bioinformatics Analysis Of Metatranscriptomesmentioning

confidence: 80%

Winter mixing impacts gene expression in marine microbial populations in the Gulf of Aqaba

Miller¹,

Pfreundt²,

Hou³

et al. 2017

Aquat. Microb. Ecol.

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“…This MGIIa_P genome together with other selected genomes were uploaded to Rapid Annotation using Subsystem Technology platform to conduct the analysis (Glass and Meyer, ). Those genomes included MG2_GG3 from surface waters of Puget Sound (Iverson et al ., ), Thalassoarchaea from the Mediterranean deep chlorophyll maximum (Martin‐Cuadrado et al ., ), 14 metagenome assembled genomes from deep‐sea waters (Li et al ., ), Thaumarchaeota isolates or enrichments (Könneke et al ., ; Hallam et al ., ; Blainey et al ., ; Kim et al ., ; Tourna et al ., ; Park et al ., ; Santoro et al ., ) and Aciduliprofundum boonei T469 (Reysenbach and Flores, ). The gene distributions in those genomes in different SEED subsystems were generated.…”

Section: Methodsmentioning

confidence: 99%

“…Two major MGII groups, MGIIa and MGIIb (Martin‐Cuadrado et al ., ), have been identified by their 16S rRNA gene (Massana et al ., ; Martin‐Cuadrado et al ., ). The availability of a number of MGII genomes has enhanced our understanding of these groups (Iverson et al ., ; Li et al ., ; Martin‐Cuadrado et al ., ). However, they are still much less known than the more thoroughly studied marine Thaumarchaeota .…”

Section: Introductionmentioning

confidence: 99%

Localized high abundance of Marine Group II archaea in the subtropical Pearl River Estuary: implications for their niche adaptation

Xie

Luo

Murugapiran

et al. 2017

Environmental Microbiology

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Marine Group II archaea are widely distributed in global oceans and dominate the total archaeal community within the upper euphotic zone of temperate waters. However, factors controlling the distribution of MGII are poorly delineated and the physiology and ecological functions of these still-uncultured organisms remain elusive. In this study, we investigated the planktonic MGII associated with particles and in free-living forms in the Pearl River Estuary (PRE) over a 10-month period. We detected high abundance of particle-associated MGII in PRE (up to ∼10 16S rRNA gene copies/l), which was around 10-fold higher than the free-living MGII in the same region, and an order of magnitude higher than previously reported in other marine environments. 10‰ salinity appeared to be a threshold value for these MGII because MGII abundance decreased sharply below it. Above 10‰ salinity, the abundance of MGII on the particles was positively correlated with phototrophs and MGII in the surface water was negatively correlated with irradiance. However, the abundances of those free-living MGII showed positive correlations with salinity and temperature, suggesting the different physiological characteristics between particle-attached and free-living MGIIs. A nearly completely assembled metagenome, MGIIa_P, was recovered using metagenome binning methods. Compared with the other two MGII genomes from surface ocean, MGIIa_P contained higher proportions of glycoside hydrolases, indicating the ability of MGIIa_P to hydrolyse glycosidic bonds in complex sugars in PRE. MGIIa_P is the first assembled MGII metagenome containing a catalase gene, which might be involved in scavenging reactive oxygen species generated by the abundant phototrophs in the eutrophic PRE. Our study presented the widespread and high abundance of MGII in the water columns of PRE, and characterized the determinant abiotic factors affecting their distribution. Their association with heterotrophs, preference for particles and resourceful metabolic traits indicate MGII might play a significant role in metabolising organic matters in the PRE and other temperate estuarine systems.

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“…A mixotrophic lifestyle for Thaumarchaeota has been inferred since the earliest reports on planktonic thaumarchaeotes described incorporation of organic carbon into signature lipids (Ingalls et al, 2006) and incorporation of labelled amino acids leucine (Ouverney and Fuhrman, 2000;Herndl et al, 2005) and aspartate (Teira et al, 2006) into single planktonic cells. Whilst initial findingsthat pure cultures of Thaumarchaeota in group I.1a (Qin et al, 2014) and group I.1b (Tourna et al, 2011) could have increased growth rates in the presence of α-keto acids and ammoniawere subsequently proven to be a result of the H 2 O 2 scavenging ability of α-keto acids (Kim et al, 2016;Qin et al, 2017), abundant genes and transcripts of S08A family serine proteases and other metallopeptidases in MG-1 deep-sea thaumarchaea have also been attributed to mixotrophic activity (Li et al, 2015). A deep sea Thaumarchaeota has also been found to encode the livFGHMK operon (Mehrshad et al, 2016), which clusters with the two sponge thaumarchaeotes (Supporting Information Fig.…”

Section: Mixotrophy Of Thaumarchaeotamentioning

confidence: 99%

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical spongeIanthella basta

Moeller

Webster

Herbold

et al. 2019

Environmental Microbiology

135

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Summary Marine sponges represent one of the few eukaryotic groups that frequently harbour symbiotic members of the Thaumarchaeota, which are important chemoautotrophic ammonia‐oxidizers in many environments. However, in most studies, direct demonstration of ammonia‐oxidation by these archaea within sponges is lacking, and little is known about sponge‐specific adaptations of ammonia‐oxidizing archaea (AOA). Here, we characterized the thaumarchaeal symbiont of the marine sponge Ianthella basta using metaproteogenomics, fluorescence in situ hybridization, qPCR and isotope‐based functional assays. ‘Candidatus Nitrosospongia ianthellae’ is only distantly related to cultured AOA. It is an abundant symbiont that is solely responsible for nitrite formation from ammonia in I. basta that surprisingly does not harbour nitrite‐oxidizing microbes. Furthermore, this AOA is equipped with an expanded set of extracellular subtilisin‐like proteases, a metalloprotease unique among archaea, as well as a putative branched‐chain amino acid ABC transporter. This repertoire is strongly indicative of a mixotrophic lifestyle and is (with slight variations) also found in other sponge‐associated, but not in free‐living AOA. We predict that this feature as well as an expanded and unique set of secreted serpins (protease inhibitors), a unique array of eukaryotic‐like proteins, and a DNA‐phosporothioation system, represent important adaptations of AOA to life within these ancient filter‐feeding animals.

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Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea

Cited by 146 publications

References 72 publications

Winter mixing impacts gene expression in marine microbial populations in the Gulf of Aqaba

Winter mixing impacts gene expression in marine microbial populations in the Gulf of Aqaba

Localized high abundance of Marine Group II archaea in the subtropical Pearl River Estuary: implications for their niche adaptation

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical spongeIanthella basta

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