Two New Beggiatoa Species Inhabiting Marine Mangrove Sediments in the Caribbean

Abstract

Beggiatoaceae, giant sulphur-oxidizing bacteria, are well known to occur in cold and temperate waters, as well as hydrothermal vents, where they form dense mats on the floor. However, they have never been described in tropical marine mangroves. Here, we describe two new species of benthic Beggiatoaceae colonizing a marine mangrove adjacent to mangrove roots. We combined phylogenetic and lipid analysis with electron microscopy in order to describe these organisms. Furthermore, oxygen and sulphide measurements in and ex situ were performed in a mesocosm to characterize their environment. Based on this, two new species, Candidatus Maribeggiatoa sp. and Candidatus Isobeggiatoa sp. inhabiting tropical marine mangroves in Guadeloupe were identified. The species identified as Candidatus Maribeggiatoa group suggests that this genus could harbour a third cluster with organisms ranging from 60 to 120 μm in diameter. This is also the first description of an Isobeggiatoa species outside of Arctic and temperate waters. The multiphasic approach also gives information about the environment and indications for the metabolism of these bacteria. Our study shows the widespread occurrence of members of Beggiatoaceae family and provides new insight in their potential role in shallow-water marine sulphide-rich environments such as mangroves.

Thioautotrophic ectosymbiosis in Pseudovorticella sp., a peritrich ciliate species colonizing wood falls in marine mangrove

“…This production of sulfur ensures the presence of sulfur-oxidizing bacteria that constitute an important food source in some shallow continental shelf systems (Montagna and Spies 1985;Pascal et al 2014;Powell et al 1983). In mangrove ecosystems, trophic resource constituted by Beggiatoa mats (Jean et al 2015) does not affect the general food web structure, meio-and macrofaunal abundances or the contribution of bacteria to their diet (Pascal et al 2014). Ectosymbiosis could be an excellent process for the host to ensure its nutrition while being able to colonize new habitats.…”

“…Samples for SEM were fixed in 0.22 m-filtered 4% paraformaldehyde solution in seawater at 4 • C. They were then dehydrated in graded concentrations of acetone, critical point dried in CO 2 and sputter-coated with gold before observation with a FEI Quanta 250 running at 20 kV (Abouna et al 2015;Jean et al 2015).…”

“…Conversely to geothermal process (Dubilier et al 2008), the debris derived from mangrove plants, algae, or sea grass may accumulate and the decomposition of this organic matter creates sulphidic habitats of various spatial and temporal extents (Ott et al 2004). This sulfur production allows the development of free-living thiotrophic bacteria (Fenchel 1994;Jean et al 2015;Jorgensen et al 2013;Stocker and Seymour 2012) or bacterial symbionts that are associated with invertebrates and ciliates both in and on the sediment (Ott et al 2004). In Guadeloupe's mangrove, endosymbiotic sulfur-oxidizing bacteria were previously described inside the gills of Phacoides pectinatus living in the sediment (Frenkiel et al 1996).…”

Temporal fluctuations in the trophic role of large benthic sulfur bacteria in mangrove sediment

“…In some places, the sediment is covered by patches of large (20-60 µm diameter) filamentous white sulfur bacteria visible with unaided eyes. Beggiatoacea bacteria belong to, at least, two genus: Maribeggiatoa and Isobeggiatoa (Jean et al, 2015). Along the year, the size of those bacterial patches is highly variable covering often several square meters.…”

First Description of Sulphur-Oxidizing Bacterial Symbiosis in a Cnidarian (Medusozoa) Living in Sulphidic Shallow-Water Environments

“…In various sulphidic environments, thioautotrophic bacteria can organize as free-living organisms in bacterial mats [ 43 – 46 ], or in chemosynthetic symbioses with diverse marine invertebrates colonizing those habitats [ 34 ]. This kind of mutualistic relationship was described later in other reducing habitats, namely shallow waters, cold seeps [ 47 , 48 ], sea-grass beds [ 49 ], whale falls [ 43 ] sunken woods [ 50 , 51 ], and organic rich mud or mangrove peat [ 36 ].…”