A Tight Interaction between the Native Seagrass Cymodocea nodosa and the Exotic Halophila stipulacea in the Aegean Sea Highlights Seagrass Holobiont Variations

Abstract

Seagrasses harbour bacterial communities with which they constitute a functional unit called holobiont that responds as a whole to environmental changes. Epiphytic bacterial communities rapidly respond to both biotic and abiotic factors, potentially contributing to the host fitness. The Lessepsian migrant Halophila stipulacea has a high phenotypical plasticity and harbours a highly diverse epiphytic bacterial community, which could support its invasiveness in the Mediterranean Sea. The current study aimed to evaluate the Halophila/Cymodocea competition in the Aegean Sea by analysing each of the two seagrasses in a meadow zone where these intermingled, as well as in their monospecific zones, at two depths. Differences in holobionts were evaluated using seagrass descriptors (morphometric, biochemical, elemental, and isotopic composition) to assess host changes, and 16S rRNA gene to identify bacterial community structure and composition. An Indicator Species Index was used to identify bacteria significantly associated with each host. In mixed meadows, native C. nodosa was shown to be affected by the presence of exotic H. stipulacea, in terms of both plant descriptors and bacterial communities, while H. stipulacea responded only to environmental factors rather than C. nodosa proximity. This study provided evidence of the competitive advantage of H. stipulacea on C. nodosa in the Aegean Sea and suggests the possible use of associated bacterial communities as an ecological seagrass descriptor.

Keywords: Indicator Species Index; biological invasion; microbiota; seagrass descriptors; seagrass interaction.

Figure 1

PCoA analysis with Bray-Curtis dissimilarity matrix of the aboveground-associated bacterial communities in site #1 (a) and #2 (b) and of the belowground-associated bacterial communities in site #1 (c) and #2 (d).

Figure 2

Venn diagram of the amplicon variant sequence (AVS) distribution on the aboveground seagrass tissues from the shallow site (#1; (a)), and the deep site (#2; (b)), or on the belowground seagrass tissues from site #1 (c) and site #2 (d).

Figure 3

Heatmap visualization of the bacterial taxa significantly associated with the aboveground or belowground plant part using the Indicator Species Index (IndVal) in each site; significant p-value (<0.05) is reported in red.

Figure 4

Seagrass pattern distribution in each sampling site: in the same meadow, a monospecific C. nodosa zone, a mixed zone, and a monospecific H. stipulacea zone can be found in a 50 m transect.

Figure 5

Sampling in the Crete Island (a); the sampling sites, Souda Bay and Mononaftis Bay (b); the sampling design, with randomly chosen sampling points (c).