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

Fusi, Marco; Booth, Jenny Marie; Marasco, Ramona; Merlino, Giuseppe; Garcias-Bonet, Neus; Barozzi, Alan; Garuglieri, Elisa; Mbobo, Tumeka; Diele, Karen; Duarte, Carlos M.; Daffonchio, Daniele

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.

Citation

Fusi, M., Booth, J. M., Marasco, R., Merlino, G., Garcias-Bonet, N., Barozzi, A., …Daffonchio, D. (2022). Bioturbation Intensity Modifies the Sediment Microbiome and Biochemistry and Supports Plant Growth in an Arid Mangrove System. Microbiology Spectrum, 10(3), https://doi.org/10.1128/spectrum.01117-22

• Journal Article Type: Article
• Acceptance Date: May 6, 2022
• Online Publication Date: Jun 1, 2022
• Publication Date: 2022
• Deposit Date: Jun 6, 2022
• Publicly Available Date: Jun 6, 2022
• Journal: Microbiology Spectrum
• Print ISSN: 2165-0497
• Publisher: American Society for Microbiology
• Peer Reviewed: Peer Reviewed
• Volume: 10
• Issue: 3
• DOI: https://doi.org/10.1128/spectrum.01117-22
• Keywords: bacterial dynamics, biochemistry, microbiome, sediment,fiddler crabs,microtidal, extreme environment, arid mangrove
• Public URL: http://researchrepository.napier.ac.uk/Output/2876309