Coastal regions experiencing declining dissolved oxygen are increasing in number and severity around the world. However, despite the importance of microbial metabolism in coastal hypoxia, few metagenomic surveys exist.
Rich geochemical datasets generated over the past 30 years have provided fine-scale resolution on the northern Gulf of Mexico (nGOM) coastal hypoxic (≤ 2 mg of O 2 L -1 ) zone. In contrast, little is known about microbial community structure and activity in the hypoxic zone despite the implication that microbial respiration is responsible for forming low dissolved oxygen (DO) conditions. Here, we hypothesized that the extent of the hypoxic zone is a driver in determining microbial community structure, and in particular, the abundance of ammonia-oxidizing archaea (AOA). Samples collected across the shelf for two consecutive hypoxic seasons in July 2013 and 2014 were analyzed using 16S rRNA gene sequencing, oligotyping, microbial co-occurrence analysis, and quantification of thaumarchaeal 16S rRNA and archaeal ammonia-monooxygenase ( amoA ) genes. In 2014 Thaumarchaeota were enriched and inversely correlated with DO while Cyanobacteria, Acidimicrobiia, and Proteobacteria where more abundant in oxic samples compared to hypoxic. Oligotyping analysis of Nitrosopumilus 16S rRNA gene sequences revealed that one oligotype was significantly inversely correlated with DO in both years. Oligotyping analysis revealed single nucleotide variation among all Nitrosopumilaceae , including Nitrosopumilus 16S rRNA gene sequences, with one oligotype possibly being better adapted to hypoxia. We further provide evidence that in the hypoxic zone of both year 2013 and 2014, low DO concentrations and high Thaumarchaeota abundances influenced microbial co-occurrence patterns. Taken together, the data demonstrated that the extent of hypoxic conditions could potentially drive patterns in microbial community structure, with two years of data revealing the annual nGOM hypoxic zone to be emerging as a low DO adapted AOA hotspot.
23 24 Running Title: 25 Microbes in 2014 nGOM hypoxic zone 26 27 Key words: 28 hypoxia, Gulf of Mexico, iTag, Thaumarchaeota, amoA, microbial community structure, 29 ammonia-oxidizing archaea (AOA) 2 30 Abstract 31 Rich geochemical datasets generated over the past 30 years have provided fine-scale resolution 32 on the northern Gulf of Mexico (nGOM) coastal hypoxic (≤ 2 mg of O 2 L -1 ) zone. In contrast, 33 little is known about microbial community structure and activity in the hypoxic zone despite the 34 implication that microbial respiration is responsible for forming low dissolved oxygen (DO) 35 conditions. Here, we hypothesized that the extent of the hypoxic zone is a driver in determining 36 microbial community structure, and in particular, the abundance of ammonia-oxidizing archaea 37 (AOA). Samples collected across the shelf for two consecutive hypoxic seasons in July 2013 and 38 2014 were analyzed using 16S rRNA gene sequencing, oligotyping, microbial co-occurrence 39 analysis and quantification of thaumarchaeal 16S rRNA and archaeal ammonia-monooxygenase 40 (amoA) genes. In 2014 Thaumarchaeota were enriched and inversely correlated with DO while 41 Cyanobacteria, Acidimicrobiia and Proteobacteria where more abundant in oxic samples 42 compared to hypoxic. Oligotyping analysis of Nitrosopumilus 16S rRNA gene sequences 43 revealed that one oligotype was significantly inversely correlated with dissolved oxygen (DO) in 44 both years and that low DO concentrations, and the high Thaumarchaeota abundances, 45 influenced microbial co-occurrence patterns. Taken together, the data demonstrated that the 46 extent of hypoxic conditions could potentially influence patterns in microbial community 47 structure, with two years of data revealing that the annual nGOM hypoxic zone is emerging as a 48 low DO adapted AOA hotspot. 49 50 51 52 3 53 Introduction 54 Deoxygenation of the ocean is one of the primary consequences of global climate change [1,2], 55 with much attention directed towards coastal hypoxic zones (dissolved oxygen (DO) 56 concentrations below 2 mg L -1 or 62.5 μmol/kg). Hypoxic zones are frequently referred to as 57 "dead zones" because they are inhospitable to macrofauna and megafauna; however, 58 microorganisms thrive in such environments [3]. Eutrophication-associated dead zones have 59 been reported in over 500 locations spanning the globe [4] and are predicted to increase in 60 number and size in the near future as a result of increasing greenhouse gas emissions [2]. The 61 northern Gulf of Mexico (nGOM) is the site of the second largest eutrophication-associated 62 coastal dead zone in the world, with bottom water hypoxia extending to over 20,000 km 2 [5] and 63 covering anywhere from 20% to 50% of the water column during the summer months [6]. The 64 nGOM hypoxic zone is influenced by the freshwater input and nutrient load from the Mississippi 65 (MI) and Atchafalaya (AR) Rivers [7], which results in a phytoplankton bloom, the biomass of 66 which is subsequently respired by aerobic microorganisms...
The northern Gulf of Mexico (nGOM) hypoxic zone is a shallow water environment where methane, a potent greenhouse gas, fluxes from sediments to bottom water and remains trapped due to summertime stratification. When the water column is destratified, an active planktonic methanotrophic community could mitigate the efflux of methane, which accumulates to high concentrations, to the atmosphere. To investigate the possibility of such a biofilter in the nGOM hypoxic zone we performed metagenome assembly, and metagenomic and metatranscriptomic read mapping. Methane monooxygenase (pmoA) was an abundant transcript, yet few canonical methanotrophs have been reported in this environment, suggesting a role for non-canonical methanotrophs. To determine the identity of these methanotrophs, we reconstructed six novel metagenome-assembled genomes (MAGs), in the Planctomycetota, Verrucomicrobiota, and one putative Latescibacterota, each with at least one pmoA gene copy. Based on ribosomal protein phylogeny, closely related microbes (mostly from Tara Oceans) and isolate genomes were selected and co-analyzed with the nGOM MAGs. Gene annotation and read mapping suggested that there is a large, diverse, and unrecognized community of active aerobic methanotrophs in the nGOM hypoxic zone and in the global ocean that could mitigate methane flux to the atmosphere.
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