Bioturbation Intensity Modifies the Sediment Microbiome and Biochemistry and Supports Plant Growth in an Arid Mangrove System

Abstract

In intertidal systems, the type and role of interactions among sediment microorganisms, animals, plants and abiotic factors are complex and not well understood. Such interactions are known to promote nutrient provision and cycling, and their dynamics and relationships may be of particular importance in arid microtidal systems characterized by minimal nutrient input. Focusing on an arid mangrove ecosystem on the central Red Sea coast, we investigated the effect of crab bioturbation intensity (comparing natural and manipulated high levels of bioturbation intensity) on biogeochemistry and bacterial communities of mangrove sediments, and on growth performance of Avicennia marina, over a period of 16 months. Along with pronounced seasonal patterns with harsh summer conditions, in which high sediment salinity, sulfate and temperature, and absence of tidal flooding occur, sediment bacterial diversity and composition, sediment physicochemical conditions, and plant performance were significantly affected by crab bioturbation intensity. For instance, bioturbation intensity influenced components of nitrogen, carbon, and phosphate cycling, bacterial relative abundance (i.e., Bacteroidia, Proteobacteria and Rhodothermi) and their predicted functionality (i.e., chemoheterotrophy), likely resulting from enhanced metabolic activity of aerobic bacteria. The complex interactions among bacteria, animals, and sediment chemistry in this arid mangrove positively impact plant growth. We show that a comprehensive approach targeting multiple biological levels provides useful information on the ecological status of mangrove forests. IMPORTANCE Bioturbation is one of the most important processes that governs sediment biocenosis in intertidal systems. By facilitating oxygen penetration into anoxic layers, bioturbation alters the overall sediment biogeochemistry. Here, we investigate how high crab bioturbation intensity modifies the mangrove sediment bacterial community, which is the second largest component of mangrove sediment biomass and plays a significant role in major biogeochemical processes. We show that the increase in crab bioturbation intensity, by ameliorating the anoxic condition of mangrove sediment and promoting sediment bacterial diversity in favor of a beneficial bacterial microbiome, improves mangrove tree growth in arid environments. These findings have significant implications because they show how crabs, by farming the mangrove sediment, can enhance the overall capacity of the system to sustain mangrove growth, fighting climate change.

Keywords: arid mangrove; bacterial dynamics; biochemistry; extreme environment; fiddler crabs; microbiome; microtidal; sediment.

FIG 1

Environmental variability at the Central Red Sea Saudi Arabia mangrove study site from May 2016 to August 2017 for deep and surface sediment. (A) Overall tidal amplitude; red line represents the locally estimated scatterplot smoothing regression to summarize the tidal inundation level across the year; (B) sediment temperature, (C) pH, and (D) salinity in surface and deep sediment. Data were not retrieved for May 2016.

FIG 2

(A) Principal coordinate analysis (PCoA) of bacterial community composition across different bioturbation intensities, depths, and months of sampling. (B to D) Canonical analysis of principal coordinates (CAP) ordination to clarify the pattern of community change in each surface sampled: surface (B, blue), subsurface (C, yellow), and deep (D, gray). (E) Overall taxonomic composition of the bacterial community at the three sampling depths (S: surface, 0 to 0.5 cm deep; SS: subsurface, 0.5 to 1.0 cm; D: deep, 5 to 5.5 cm) across sampling times at two different levels of bioturbation intensity (normal and high-intensity bioturbation).

FIG 3

Top 30 identity operational taxonomic units (OTUs) used to discriminate bacterial communities in surface, subsurface, and deep sediment at different levels of bioturbation intensity across the sampling season. The assigned taxonomy of each taxon is displayed at the class level. Bar plots show the importance values of each OTU, estimated by random forest model as Mean Decrease Accuracy (%IncMSE).

FIG 4

Avicennia marina performance during the survey period: (A and B) number of pneumatophores, (C and D) tree height, and (E and F) branch diameter are reported as indicators of plant growth and development in high and normal bioturbation intensity. The graphs in panels A, C, and E (boxplots and notches) describe the growth of the plants over the duration of the experiment at highly and normal bioturbation intensity. Graphs in panels B, D, and F show plant growth over the duration of the experiment, represented as a function of the days, with trendlines for high and normal bioturbation intensities.

FIG 5

Structural equation model assessing the effects of the studied factors on plant performance. Numbers superimposed on the arrows in boxes reflect the strength of the effect of each variable. Only significant effects (P < 0.05) are shown. The model was satisfactorily fitted to the data, as suggested by the non-significant χ² values, root mean square error of approximation value of 0.092, and CFI value of 0.89. The strength of correlations between bioturbation intensity and the different parameters studied are reflected in the different size of the arrows, which are proportional to the Mantel statistic R values based on the Pearson’s correlation. Mangrove ecosystems are densely colonized by burrowing fauna, which have a significant impact on sediment physicochemical conditions (SPC). In particular, TPC, particulate organic carbon (POC), particulate organic nitrogen (PON), particulate inorganic nitrogen (PIN), nitrate, nitrite, and phosphate were the main variables affected by the crabs. By aerating, mixing, and modifying the sediment structure, bioturbation affects the physicochemical properties of the soil and its sediment bacterial community (SBC), including the alpha and beta diversity and the quantity of 16S rRNA gene copies. These three variables also significantly affected plant growth. Among the sediment chemical parameters, TPC, PON, and particulate inorganic carbon (PIC) significantly affected plant growth. Ultimately, a significant effect of bioturbation intensity on the plant growth was revealed, showing that crab bioturbation (CB) sustained plant performance (PGD) in particularly stressful situations, such as those in arid environments.