Drying effects on archaeal community composition and methanogenesis in bromeliad tanks

Abstract

Tank bromeliads are highly abundant epiphytes in neotropical forests and form a unique canopy wetland ecosystem which is involved in the global methane cycle. Although the tropical climate is characterized by high annual precipitation, the plants can face periods of restricted water. Thus, we hypothesized that water is an important controller of the archaeal community composition and the pathway of methane formation in tank bromeliads. Greenhouse experiments were established to investigate the resident and active archaeal community targeting the 16S rDNA and 16S rRNA in the tank slurry of bromeliads at three different moisture levels. Archaeal community composition and abundance were determined using terminal restriction fragment length polymorphism and quantitative PCR. Release of methane and its stable carbon isotopic signature were determined in a further incubation experiment under two moisture levels. The relative abundance of aceticlastic Methanosaetaceae increased up to 34% and that of hydrogenotrophic Methanobacteriales decreased by more than half with decreasing moisture. Furthermore, at low moisture levels, methane production was up to 100-fold lower (≤0.1-1.1 nmol gdw(-1) d(-1)) than under high moisture levels (10-15 nmol gdw(-1) d(-1)). The rapid response of the archaeal community indicates that the pathway of methane formation in bromeliad tanks may indeed be strongly susceptible to periods of drought in neotropical forest canopies.

Bromeliad tanks are unique habitats for microbial communities involved in methane turnover

“…In former studies this TRF was assigned to the hydrogenotrophic methanogens Methanomicrobiales or Methanocellales (Brandt et al 2014;Martinson et al 2010). The methanotrophic community was dominated by a 245-bp TRF (Supplementary Fig.…”

“…Carbon availability was already identified as one of the main drivers of microbial community structure in soil (Fierer et al 2003) and Lopez et al (2009) assumed that occasional organic matter inputs can induce a eutrophic condition in tank-bromeliads. In a previous study by Goffredi et al (2011b) it was shown that pH has an effect on the bacterial community composition and that a low water content and therefore an increased oxygen exposure, affected the bacterial and archaeal community composition in tank bromeliad slurry (Brandt et al 2014;Brandt 2015). In the present study, the microbial communities were further sorted along nitrogen concentrations in the tank slurry.…”

“…With the addition of 1 % CH 4 we solely targeted low-affinity methanotrophs that are adapted to grow at high CH 4 concentrations (Dunfield 2007). Along with dry periods methane emission decreases in tank slurries (Brandt et al 2014) that may also favor the activity of high-affinity methanotrophs in bromeliad tanks. Epiphytic bromeliads increase the volume of arboreal carbon storage by creating catchments in which litter accumulates until it is decomposed (Nadkarni 1994).…”

“…In contrast to other studies, which lasted up to years (Carrias et al 2001;Goffredi et al 2011b;Carmo et al 2014), our study captured only a snapshot in time. However it is to be emphasized, that due to different water availabilities the microbial community composition in tank slurry can dramatically change even within days (Brandt et al 2014). Here, all tank slurry samples were taken within three days to limit further variations (e.g.…”

“…On the one hand this can be due to environmental factors that were not measured, such as water volume which was shown to affect invertebrate diversity and the archaeal and bacterial community composition and the pathway of methane formation in tank bromeliads (Dézerald et al 2014;Brandt et al 2014;Brandt 2015). On the other hand there is probably a large stochastic component connected with the ephemerality of the plants and dispersal dynamics (Farjalla et al 2012;Jocque and Field 2014).…”