The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation

PLoS One. 2015 Jun 23;10(6):e0130116. doi: 10.1371/journal.pone.0130116. eCollection 2015.

Abstract

Objectives: The marine benthic nitrogen cycle is affected by both the presence and activity of macrofauna and the diversity of N-cycling microbes. However, integrated research simultaneously investigating macrofauna, microbes and N-cycling is lacking. We investigated spatio-temporal patterns in microbial community composition and diversity, macrofaunal abundance and their sediment reworking activity, and N-cycling in seven subtidal stations in the Southern North Sea.

Spatio-temporal patterns of the microbial communities: Our results indicated that bacteria (total and β-AOB) showed more spatio-temporal variation than archaea (total and AOA) as sedimentation of organic matter and the subsequent changes in the environment had a stronger impact on their community composition and diversity indices in our study area. However, spatio-temporal patterns of total bacterial and β-AOB communities were different and related to the availability of ammonium for the autotrophic β-AOB. Highest bacterial richness and diversity were observed in June at the timing of the phytoplankton bloom deposition, while richness of β-AOB as well as AOA peaked in September. Total archaeal community showed no temporal variation in diversity indices.

Macrofauna, microbes and the benthic n-cycle: Distance based linear models revealed that, independent from the effect of grain size and the quality and quantity of sediment organic matter, nitrification and N-mineralization were affected by respectively the diversity of metabolically active β-AOB and AOA, and the total bacteria, near the sediment-water interface. Separate models demonstrated a significant and independent effect of macrofaunal activities on community composition and richness of total bacteria, and diversity indices of metabolically active AOA. Diversity of β-AOB was significantly affected by macrofaunal abundance. Our results support the link between microbial biodiversity and ecosystem functioning in marine sediments, and provided broad correlative support for the hypothesis that this relationship is modulated by macrofaunal activity. We hypothesized that the latter effect can be explained by their bioturbating and bio-irrigating activities, increasing the spatial complexity of the biogeochemical environment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Geologic Sediments / microbiology*
  • Marine Biology*
  • Microbiota*
  • Nitrogen / metabolism*

Substances

  • Nitrogen

Grants and funding

This work was supported by the Ministry of Science, Research and Technology, Iran (http://www.msrt.ir/fa/pages/Home.aspx#) scholarship nr 24-88200022; Recipient: MYF. UB was supported by FWO Project No. G.0033.11. This work was also supported by the Special Research Fund of Ghent University (BOF-GOA 01GA1911W). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.