Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California

Abstract

Whale-falls represent localized areas of extreme organic enrichment in an otherwise oligotrophic deep-sea environment. Anaerobic remineralization within these habitats is typically portrayed as sulfidogenic; however, we demonstrate that these systems are also favorable for diverse methaneproducing archaeal assemblages, representing up to 40% of total cell counts. Chemical analyses revealed elevated methane and depleted sulfate concentrations in sediments under the whale-fall, as compared to surrounding sediments. Carbon was enriched (up to 3.5%) in whale-fall sediments, as well as the surrounding sea floor to at least 10 m, forming a 'bulls eye' of elevated carbon. The diversity of sedimentary archaea associated with the 2893 m whale-fall in Monterey Canyon (California) varied both spatially and temporally. 16S rRNA diversity, determined by both sequencing and terminal restriction fragment length polymorphism analysis, as well as quantitative PCR of the methyl-coenzyme M reductase gene, revealed that methanogens, including members of the Methanomicrobiales and Methanosarcinales, were the dominant archaea (up to 98%) in sediments immediately beneath the whale-fall. Temporal changes in this archaeal community included the early establishment of methylotrophic methanogens followed by development of methanogens thought to be hydrogenotrophic, as well as members related to the newly described methanotrophic lineage, ANME-3. In comparison, archaeal assemblages in 'reference' sediments collected 10 m from the whale-fall primarily consisted of Crenarchaeota affiliated with marine group I and marine benthic group B. Overall, these results indicate that whale-falls can favor the establishment of metabolically and phylogenetically diverse methanogen assemblages, resulting in an active near-seafloor methane cycle in the deep sea.

Distributions of putative aerobic methanotrophs in diverse pelagic marine environments

“…Semi-nested amplification was necessary to improve specificity for the pmo spacer in samples in which the target was in low abundance (less than B200 copies per ng environmental DNA, typical of non-methane seep environments). Approximately 100 ng of fluorescent PCR product was precipitated and separated through capillary electrophoresis as described for terminal restriction fragment length polymorphism analysis in Goffredi et al (2008). Electropherogram peaks were analyzed in a targeted range (B400-650 base pairs (bp)), as determined by the in silico and empirical spacer lengths of OPU1, OPU3, Group X and spacer lengths from currently described cultured organisms (Table 1).…”

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

“…These spatially heterogeneous and enriched habitats persist for varying timespans of 5 to 50 years, depending on a number of conditions (for example, depth and oxygen concentrations; Smith and Baco, 2003;Goffredi et al, 2004;Braby et al, 2007;Lundsten et al, 2010). Many organisms, both animals and free-living microbes, tend to be stratified in space and time around the decomposing carcasses (Smith et al, 2002;Goffredi et al, 2004;Braby et al, 2007;Goffredi et al, 2008;Vrijenhoek et al, 2009;Goffredi and Orphan, 2010;Lundsten et al, 2010). Temporal variation also exists in relative abundances of the dominant symbiont types that infect Osedax (Goffredi et al, 2007;Verna et al, 2010).…”

“…Targeted PCR amplification of the soxB from the genomic DNA of symbiont Rs2, and not Rs1, confirmed the likely absence of these genes from the latter symbiont (Supplementary Figure S4). Advanced stages of whale fall decomposition generate significant increases in sulfide concentrations (Smith and Baco, 2003;Goffredi et al, 2008) and the ability to detoxify this harmful substance should benefit Rs2 during these later stages. Rs1 and Rs2 also differ in their abilities to use carbohydrates (Tables 3 and 4).…”

Biogeochemistry of a deep-sea whale fall: sulfate reduction, sulfide efflux and methanogenesis

“…Sediments surrounding whale carcasses are enriched with lipids and other organic compounds derived from the carcass (Naganuma et al 1996. The organic enrichment causes anoxic conditions in the sediment, due to high microbial oxygen consumption (Allison 1988, Allison et al 1991, and favors anaerobic processes such as SR and methanogenesis (MG) (Goffredi et al 2008) -processes which usually play a minor role in the carbon cycling of organic-poor, deep-sea sediments (Wenzhöfer & Glud 2002 and references therein). Chemosynthetic sulfide-oxidizing microorganisms found at whale falls include free-living, mat-forming bacteria (e.g.…”