Microbial megacities fueled by methane oxidation in a mineral spring cave

Abstract

Massive biofilms have been discovered in the cave of an iodine-rich former medicinal spring in southern Germany. The biofilms completely cover the walls and ceilings of the cave, giving rise to speculations about their metabolism. Here we report on first insights into the structure and function of the biofilm microbiota, combining geochemical, imaging and molecular analytics. Stable isotope analysis indicated that thermogenic methane emerging into the cave served as an important driver of biofilm formation. The undisturbed cavern atmosphere contained up to 3000 p.p.m. methane and was microoxic. A high abundance and diversity of aerobic methanotrophs primarily within the Methylococcales (Gammaproteobacteria) and methylotrophic Methylophilaceae (Betaproteobacteria) were found in the biofilms, along with a surprising diversity of associated heterotrophic bacteria. The highest methane oxidation potentials were measured for submerged biofilms on the cavern wall. Highly organized globular structures of the biofilm matrix were revealed by fluorescent lectin staining. We propose that the extracellular matrix served not only as an electron sink for nutrient-limited biofilm methylotrophs but potentially also as a diffusive barrier against volatilized iodine species. Possible links between carbon and iodine cycling in this peculiar habitat are discussed.

Analysis of viral and bacterial communities in groundwater associated with contaminated land

“…Abundant members found within sampled bacterial communities that have been linked to methanogenesis include, the actinobacterial order OPB41 (Robbins et al, 2016), the Methylophilales order (Redmond et al, 2010), Porphyromonadaceae (Wang et al, 2016), Hyphomicrobiaceae (Beck et al, 2013;Karwautz et al, 2018;Osaka et al, 2008) and Syntrophaceae (Gray et al, 2011). Porphyromonadaceae was found particularly abundant in C1 (4.29-15.49%) and C2 communities (23.44%)…”

Natural Selection in Synthetic Communities Highlights the Roles of Methylococcaceae and Methylophilaceae and Suggests Differential Roles for Alternative Methanol Dehydrogenases in Methane Consumption

“…In accordance with this model, methanotrophs feed methanol to methanol utilizers, and both methanotrophs and methanol utilizers produce organics that feed non-methylotrophic heterotrophs, in conjunction with denitrification. In accordance with the model, methanol should be available to all organisms that are capable of methanol utilization, and other organics should be available to all heterotrophs, as “public goods.” However, experimental evidence is somewhat contradictory to the notion of “public goods,” as specific species cooccurrences, such as cooperative behavior of Methylococcaceae and Methylophilaceae , have been noted not only in manipulated microcosms ( Kalyuzhnaya et al, 2008 ; Beck et al, 2013 ; Hernandez et al, 2015 ; Oshkin et al, 2015 ), but also in natural populations inhabiting methane-rich environments such as permafrosts ( Martineau et al, 2010 ; Crevecoeur et al, 2015 ) or methane-fueled cave biofilms ( Karwautz et al, 2017 ). These results suggest either that many species detected in natural niches, through DNA profiling, are dormant, that some organisms may be more competitive for “public goods,” or that specific partnerships are taking place.…”

Microbial Ecology of Methanotrophy in Streams Along a Gradient of CH4 Availability

“…Although numerically not abundant in many environments, they functionally dominate MOX when CH 4 concentrations are high. Recent studies revealed the importance of Crenothrix, a filamentous type I MOB in lakes (Oswald et al, 2017) and caves (Karwautz et al, 2018). In contrast, α-proteobacterial MOB typically feature more stable populations with less responsiveness to fluctuating CH 4 concentrations (Ho et al, 2013).…”