Carbon sources of benthic fauna in temperate lakes across multiple trophic states

Abstract

Abstract. Previous studies have shown that microbially produced methane can be a dominant carbon source of lacustrine sedimentary macrofauna in eutrophic lakes, most likely through grazing on methane-oxidizing bacteria. Here we investigate the contributions of different carbon sources to macrofaunal biomass across five lakes in central Switzerland that range from oligotrophic to highly eutrophic. Macrofaunal communities change with trophic state, with chironomid larvae dominating oligotrophic and tubificid oligochaetes dominating eutrophic lake sediments. The 13C-isotopic data suggest that the average contribution of methane-derived carbon to the biomass of both macrofaunal groups is similar but consistently remains minor, ranging from only ∼1 % in the oligotrophic lake to at most 12 % in the eutrophic lakes. The remaining biomass can be explained by the assimilation of detritus-derived organic carbon. Low abundances of methane-cycling microorganisms in macrofaunal specimens, burrows, and surrounding sediment based on 16S ribosomal RNA (rRNA) gene sequences and copy numbers of genes involved in anaerobic and aerobic methane cycling (mcrA, pmoA) support the interpretation of isotopic data. Notably, 16S rRNA gene sequences of macrofauna, including macrofaunal guts, are highly divergent from those in tubes or sediments. Many macrofaunal specimens are dominated by a single 16S rRNA phylotype of Fusobacteria, α-, β-, γ-, or ε-Proteobacteria, Bacteroidetes, or Parcubacteria. This raises the question of whether dominant lake macrofauna live in so far uncharacterized relationships with detrital organic-matter-degrading bacterial endosymbionts.

Redox Zone and Trophic State as Drivers of Methane-Oxidizing Bacterial Abundance and Community Structure in Lake Sediments

“…due to viral lysis or predation. Though we lack data on viral lysis rates, previous work has shown high abundances of oligochaetes (Tubificidae) to 20 cm sediment depth in the three eutrophic lakes and absence of these worms from all but the sediment surface in Lake Lucerne (Fiskal et al, 2021a). Gut microbiome analyses suggest protein-rich diets that are consistent with microbial grazing as a major food source of tubificids (Fiskal et al, 2021a;de Valk et al, 2017).…”

“…Though we lack data on viral lysis rates, previous work has shown high abundances of oligochaetes (Tubificidae) to 20 cm sediment depth in the three eutrophic lakes and absence of these worms from all but the sediment surface in Lake Lucerne (Fiskal et al, 2021a). Gut microbiome analyses suggest protein-rich diets that are consistent with microbial grazing as a major food source of tubificids (Fiskal et al, 2021a;de Valk et al, 2017). While lake sedimentary invertebrates are known to stimulate growth of MOB in surface sediments ("microbial gardening"), leading to MOB becoming a major food source of these invertebrates in some lakes (Kiyashko et al, 2001;Deines et al, 2007;Jones and Grey, 2011), none of the stations in this study show evidence for MOB gardening (Fiskal et al, 2021a).…”

“…LEICAS was initiated in 2016, when Lake Lucerne, Lake Zurich, Lake Zug, Lake Baldegg, and Lake Greifen were each sampled at three stations that covered a water depth gradient from shallow sublittoral to profundal sediments. Biogeochemical, organic geochemical, and 16S rRNA gene-based microbiological data on all stations were published previously by Fiskal et al (2019Fiskal et al ( , 2021a and Han et al (2020). An experimental study to investigate impacts of lake "oligotrophication" on sedimentary processes has also been published (Fiskal et al 2021b).…”

“…Bottom water temperatures at the time of sampling were 6-7 °C at all stations except the shallow (9 °C) and deep stations (5 °C) in Lake Lucerne. All sites were bioturbated and contained benthic infaunal chironomids and/or oligochaetes (Fiskal et al, 2021a), except the deep, permanently hypoxic station in Lake Zurich. Sediment porewater for downstream measurements of dissolved electron acceptors (nitrate, sulfate, dissolved inorganic carbon) and respiration end products (Mn 2+ , Fe 2+ , ammonium) was sampled using rhizons (0.2 μm pore size, Rhizosphere) from a designated core with pre-drilled holes that were taped prior to coring.…”

“…Lake baldegg (eutrophic) Lake zug (eutrophic) Lake zurich (mesotrophic) Lake lucerne (oligotrophic) Aerobic 0-0.17 ± 0.03 0-0.08 ± 0.02 0-0.23 ± 0.03 0-0.22 ± 0.08 0-0.73 ± 0.25 Denitrification 0-2.5 ± 1.0 0-2.8 ± 1.2 0-7.7 ± 3.1 0-3.3 ± 1.4 0-9.0 ± 2.0 Sulfate reduction 0-5.8 ± 2.0 0-6.2 ± 3.3 0-11.7 ± 3.1 0-10.3 ± 1.2 0-11.0 ± 2.0 Mn(IV) reduction 0.3 ± 0.3-8.2 ± 4.9 0.3 ± 0.3-14 ± 7 0.5 ± 0.0-5.0 ± 0.0 0.3 ± 0.3-24 ± 15 0.7 ± 0.8-bottom Fe(III) reduction 0.5 ± 0.0-bottom throughout 0.5 ± 0.0-bottom 0.5 ± 0.0-bottom 0.8 ± 0.6-bottom Methanogenesis throughout throughout throughout 2.6 ± 2.4-bottom 3.0 ± 1.7-bottom community analyses, and sedimentological analyses (including Cs-137 and unsupported Pb-210 for sediment dating; further details and data in Fiskal et al (2019Fiskal et al ( , 2021a).…”