Carbon fixation by basalt-hosted microbial communities

Abstract

Oceanic crust is a massive potential habitat for microbial life on Earth, yet our understanding of this ecosystem is limited due to difficulty in access. In particular, measurements of rates of microbial activity are sparse. We used stable carbon isotope incubations of crustal samples, coupled with functional gene analyses, to examine the potential for carbon fixation on oceanic crust. Both seafloor-exposed and subseafloor basalts were recovered from different mid-ocean ridge and hot spot environments (i.e., the Juan de Fuca Ridge, the Mid-Atlantic Ridge, and the Loihi Seamount) and incubated with 13C-labeled bicarbonate. Seafloor-exposed basalts revealed incorporation of 13C-label into organic matter over time, though the degree of incorporation was heterogeneous. The incorporation of 13C into biomass was inconclusive in subseafloor basalts. Translating these measurements into potential rates of carbon fixation indicated that 0.1–10 nmol C g-1rock d-1 could be fixed by seafloor-exposed rocks. When scaled to the global production of oceanic crust, this suggests carbon fixation rates of 109–1012 g C year-1, which matches earlier predictions based on thermodynamic calculations. Functional gene analyses indicate that the Calvin cycle is likely the dominant biochemical mechanism for carbon fixation in basalt-hosted biofilms, although the reductive acetyl-CoA pathway and reverse TCA cycle likely play some role in net carbon fixation. These results provide empirical evidence for autotrophy in oceanic crust, suggesting that basalt-hosted autotrophy could be a significant contributor of organic matter in this remote and vast environment.

Assessing Microbial Community Patterns During Incipient Soil Formation From Basalt

“…Phylogenetic analysis of OTUs revealed Proteobacteria to be the dominant phylum in the system, an observation reported commonly for soils (Janssen, ) and seafloor basalts (Cockell et al, ; Orcutt et al, ; Singer et al, ). However, the surface samples more closely resembled oligotrophic community composition, with high relative abundance of Actinobacteria , as previously observed in other studies (Neilson et al, , ).…”

“…The key enzyme for reverse TCA cycle, citrate lyase, could not be predicted though counts of other TCA cycle enzymes (methylisocitrate lyase and isocitrate lyase) were predicted (Supporting Information Figure S8). These genes were of interest due to their presence in seafloor basalt (Orcutt et al, ). An alphaproteobacterial methanotroph, Methylocystaceae (0.1%), was also observed across the depth profile.…”

“…Actinobacterial phyla have also been reported to scavenge atmospheric hydrogen in dry and hot oligotrophic environments (Greening et al, ; Lynch et al, ) and could potentially be carbon‐fixation strategy employed in miniLEO surficial layer. Surprisingly, photoautotrophic Cyanobacteria, generally found in basalt environments (Olsson‐Francis et al, ; Orcutt et al, , ; Singer et al, ) was not an abundant phylum in miniLEO. The glass‐enclosed structure of Biosphere 2 may either have filtered out necessary UV wavelengths required for cyanobacterial growth or sensitivity to incoming UV radiation may have driven these groups to move to areas with less light penetration at the cost of reduced cellular growth and productivity (Bebout & Garcia‐pichel, ).…”

Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust

“…Despite the potentially global importance of microbial life within the upper crust, fundamental questions regarding cellular recruitment, extent of activity, niche partitioning, and community succession in this habitat remain unanswered. There have been only a few published studies dedicated to microbial interrogation of native subseafloor crustal rocks (1,(14)(15)(16)(17) and even fewer that have addressed the potential biogeochemical functions of these communities (16,18). Based on the limited body of literature, it appears that microbial communities in the subseafloor crust are unique in comparison to those found in hydrothermal plumes, deep seawater, and hydrothermal fluids and in seafloor exposed basalt (12) and the overlying sediments (19).…”

“…For characterization of AOA communities at high taxonomic resolution, we used two phylogenetic markers, i.e., archaeal 16S rRNA and amoA genes, whose phylogenies are congruent down to at least the taxonomic rank of order (28,29) and can be reliably used to distinguish environmentally relevant suborder clades (30). We also explored the possibility of in situ nitrification within the upper ocean crust using a hydrogeological box model (14) based on the basal sediment geochemistry.…”