The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

Abstract

Microorganisms mediate geochemical processes in deep-sea hydrothermal vent plumes, which are a conduit for transfer of elements and energy from the subsurface to the oceans. Despite this important microbial influence on marine geochemistry, the ecology and activity of microbial communities in hydrothermal plumes is largely unexplored. Here, we use a coordinated metagenomic and metatranscriptomic approach to compare microbial communities in Guaymas Basin hydrothermal plumes to background waters above the plume and in the adjacent Carmen Basin. Despite marked increases in plume total RNA concentrations (3-4 times) and microbially mediated manganese oxidation rates (15-125 times), plume and background metatranscriptomes were dominated by the same groups of methanotrophs and chemolithoautotrophs. Abundant community members of Guaymas Basin seafloor environments (hydrothermal sediments and chimneys) were not prevalent in the plume metatranscriptome. De novo metagenomic assembly was used to reconstruct genomes of abundant populations, including Marine Group I archaea, Methylococcaceae, SAR324 Deltaproteobacteria and SUP05 Gammaproteobacteria. Mapping transcripts to these genomes revealed abundant expression of genes involved in the chemolithotrophic oxidation of ammonia (amo), methane (pmo) and sulfur (sox). Whereas amo and pmo gene transcripts were abundant in both plume and background, transcripts of sox genes for sulfur oxidation from SUP05 groups displayed a 10-20-fold increase in plumes. We conclude that the biogeochemistry of Guaymas Basin hydrothermal plumes is mediated by microorganisms that are derived from seawater rather than from seafloor hydrothermal environments such as chimneys or sediments, and that hydrothermal inputs serve as important electron donors for primary production in the deep Gulf of California.

Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume

“…The balance of DNA reads in background versus plume was more variable, and in some cases, much higher in background than plume (Supplementary Figure S3). In terms of the whole community, these MGI small subunit (SSU) rRNA genes were the most abundantly represented Archaea in both plume and background metatranscriptomic data sets (Lesniewski et al, 2012).…”

“…Once on deck, plume and background waters were immediately filtered by N 2 gas pressure onto 0.2-mm pore size, 142-mm diameter polycarbonate filters, and fixed and frozen in RNAlater as previously described (Dick et al, 2009b;Dick and Tebo, 2010). Further details of sample processing, locations and environmental conditions are provided in Supplementary Table S1 and in Lesniewski et al (2012). Plume-1 and Plume-2 were used for genomics, whereas Plume-3 and Plume-4 were transcriptomics samples from the plume.…”

“…Two background samples were each used for both metagenomics and metatranscriptomics. As it is not possible to obtain true background samples from sub-sill depths of the GB, Background-1 was taken from just above the GB plume and Background-2 was from the next basin south of Guaymas, Carmen Basin (Lesniewski et al, 2012).…”

A new class of marine Euryarchaeota group II from the mediterranean deep chlorophyll maximum

“…To compare the results among the different data sets, the number of reads was normalized considering the size of the contig and of the collection (number of reads per kilobase per gigabase of the collection). The meso and bathypelagic metagenome collections screened were: Marmara Sea-1000 m (Quaiser et al, 2011), Matapan-Vavilov Deep in the Mediterranean Sea-4900 m (Smedile et al, 2012), North Pacific subtropical gyre-ALOHA station-4000 m (Konstantinidis et al, 2009), Guaymas Basin hydrothermal vent in the Gulf of California (Lesniewski et al, 2012) and a metagenome obtained at 800 m in the South Atlantic Gyre (Swan et al, 2014).…”

Significance of archaeal nitrification in hypoxic waters of the Baltic Sea

“…These studies often revealed the dominance of archaeal over bacterial ammonia oxidizers (Francis et al, 2005;Wuchter et al, 2006;Mincer et al, 2007;Agogué et al, 2008;Newell et al, 2013). Further support for the strong role for AOA in nitrification comes from observations of the co-occurrence of archaeal amoA in areas of nitrification activity (Caffrey et al, 2007;Beman et al, 2008;Alves et al, 2013) and from metatranscriptomic studies (Baker et al, 2012;Lesniewski et al, 2012). However, to determine the actual contribution and impact of AOA on the nitrogen cycle requires measurements of ammonium oxidation rates, as they cannot be deduced from transcript abundance alone (Mu mann et al, 2011), given that quantification is influenced by, for example, mRNA degradation during sampling (Feike et al, 2012) and, in addition, may not inevitably reflect environmental activity.…”