**4.3 The sponge holobiont**

#### **4.3.1 Sponges shelter complex consortia of microorganisms, akin to some biofilms**

Modern reef-dwelling sponges are studied as important contributors to the constructive and bioerosive dynamics of limestone scaffolds in shallow tropical waters, but the main interest in them lies in their ability to harbor highly complex communities of micro- and macroorganisms. The overall sponge-associated microbial component is extremely diverse, bacteria alone representing up to half of the sponge biomass and occurring everywhere within their host, often as consortia. Only a very small percentage of these bacteria have been cultured in isolation. The term bacteriosponge (Reiswig, 1981) reflects the uniqueness of this prokaryotic-eukaryotic functional consortium, the holobiome being the sum total of all associated microbial components.

The demosponge microbiome occasionally includes zooxanthellae (Weisz et al., 2010) that share surface cortical layers with cyanobacteria (Li, 2009), while the eubacteria and archeae typically dominate the inner regions. Cyanobacteria can be extremely abundant within their host and provide them with competitive advantages (cyanobacteriosponges *Aphanocapsa raspaigellae* in *Tersiops hoshinota*, König et al., 2006). Some unicellular strains are widely distributed across sponge hosts and reef localities, e.g. *Synechococcus spongiarum* which is regarded as a generalist (Erwin & Thacker, 2008). Sponge-specific clades of filamentous cyanobacteria, on the other hand, suggest unique coevolutionary histories (Thacker & Starnes, 2003; Hill et al., 2006) which provide greater benefit to their hosts (Thacker, 2005). Symbiotic cyanobacteria, situated both intercellularly and intracellularly, have been reported in a large variety of marine sponges (Thajuddin et al., 2005; Usher, 2008).

#### **4.3.2 Sponges with different life strategies host different bacterial populations**

Demosponge microbiologists have contrasted species that form dense and phylogenetically complex microbial communities (HMA or high microbial abundance) against those that contain only few and less diverse microbes of essentially non-specific types (LMA or low microbial abundance), representing two different basic life strategies (Weisz et al., 2008). HMA sponges typically have a reduced aquiferous system with lower pumping rates, while LMA sponges have highly porous tissues with high pumping rates that enable rapid uptake of small particulate organic matter, yet the nitrification/denitrification rates remain comparable (Schlappy et al., 2010). Calcareous sponges have been comparatively less studied as regards their bacterial flora. Quévrain et al. (2009) and Roué et al. (2010) found that two North Atlantic calcareous species had a stable bacterial population throughout the year.

#### **4.3.3 Specificity, host selectivity and vertical transmission to offspring**

Bacterial associations may range from non-specific commensalism to species-specific symbiosis, with some intracellular or even endonuclear examples which are more common in protistan hosts than in metazoans in which they are regarded as signs of a very ancient association (see Hoyos, 2010). In sponges **(**Vacelet, 1970; Friedrich et al., 1999), such intranuclear examples are found in the genus *Aplysina*. More commonly, the existence of

and disease (Webster et al., 2011), and tolerance to eutrophication (Turque et al., 2010). Garderes et al. (2011) showed that specific bacterial quorum sensing signals can be recognized by sponge cells, triggering phagocytosis, a response proposed as part of a

**4.3.1 Sponges shelter complex consortia of microorganisms, akin to some biofilms**  Modern reef-dwelling sponges are studied as important contributors to the constructive and bioerosive dynamics of limestone scaffolds in shallow tropical waters, but the main interest in them lies in their ability to harbor highly complex communities of micro- and macroorganisms. The overall sponge-associated microbial component is extremely diverse, bacteria alone representing up to half of the sponge biomass and occurring everywhere within their host, often as consortia. Only a very small percentage of these bacteria have been cultured in isolation. The term bacteriosponge (Reiswig, 1981) reflects the uniqueness of this prokaryotic-eukaryotic functional consortium, the holobiome being the sum total of

The demosponge microbiome occasionally includes zooxanthellae (Weisz et al., 2010) that share surface cortical layers with cyanobacteria (Li, 2009), while the eubacteria and archeae typically dominate the inner regions. Cyanobacteria can be extremely abundant within their host and provide them with competitive advantages (cyanobacteriosponges *Aphanocapsa raspaigellae* in *Tersiops hoshinota*, König et al., 2006). Some unicellular strains are widely distributed across sponge hosts and reef localities, e.g. *Synechococcus spongiarum* which is regarded as a generalist (Erwin & Thacker, 2008). Sponge-specific clades of filamentous cyanobacteria, on the other hand, suggest unique coevolutionary histories (Thacker & Starnes, 2003; Hill et al., 2006) which provide greater benefit to their hosts (Thacker, 2005). Symbiotic cyanobacteria, situated both intercellularly and intracellularly, have been

reported in a large variety of marine sponges (Thajuddin et al., 2005; Usher, 2008).

**4.3.2 Sponges with different life strategies host different bacterial populations** 

calcareous species had a stable bacterial population throughout the year.

**4.3.3 Specificity, host selectivity and vertical transmission to offspring** 

Demosponge microbiologists have contrasted species that form dense and phylogenetically complex microbial communities (HMA or high microbial abundance) against those that contain only few and less diverse microbes of essentially non-specific types (LMA or low microbial abundance), representing two different basic life strategies (Weisz et al., 2008). HMA sponges typically have a reduced aquiferous system with lower pumping rates, while LMA sponges have highly porous tissues with high pumping rates that enable rapid uptake of small particulate organic matter, yet the nitrification/denitrification rates remain comparable (Schlappy et al., 2010). Calcareous sponges have been comparatively less studied as regards their bacterial flora. Quévrain et al. (2009) and Roué et al. (2010) found that two North Atlantic

Bacterial associations may range from non-specific commensalism to species-specific symbiosis, with some intracellular or even endonuclear examples which are more common in protistan hosts than in metazoans in which they are regarded as signs of a very ancient association (see Hoyos, 2010). In sponges **(**Vacelet, 1970; Friedrich et al., 1999), such intranuclear examples are found in the genus *Aplysina*. More commonly, the existence of

symbiont population-regulating mechanism.

**4.3 The sponge holobiont** 

all associated microbial components.

core-consortia of bacteria which are found in distant conspecific sponge populations and all year around indicates a high degree of functional specificity and species selectivity. Vertical transmission of "essential" bacteria from parent to offspring via the eggs or the larvae in, respectively, oviparous and ovoviviparous species have been investigated by Webster et al. (2010b) in major poriferan clades: Demospongiae, Homoscleromorpha, Calcarea and Hexactinellida (Ereskovsky, 2011), also including cyanobacteria (Usher et al., 2001).

### **4.3.4 Other components of the sponge holobiont**

Archaea are found in a wide variety of sponges, and their populations have been characterized in several taxa, e.g. *Axinella*, either as clade-specific mutualists or not, with some sponges lacking them altogether (Holmes & Blanch, 2007). This understudied component is primarily involved in ammonia oxidation, but the co-production of bioactive metabolites is not excluded.

In addition, sponges are host to microscopic algae, viruses, yeast and fungi, which add to the biodiversity and, at least for the fungi, to the chemodiversity of the holobiome (e.g. König et al., 2006). Sponges are host to a strain of *Aspergillus sydowii*, a fungus which has been identified as a causative agent of epidemics that affect gorgonian corals. The authors of the study (Ein-Gil et al., 2009) postulate that sponges may act as reservoirs of potential marine pathogens, in the same way as the bacterial populations associated with turf and macroalgae are considered as potential sources of infection to scleractinian corals which are host to specific microbiomes (Barott et al., 2009).

Polychaetes, prosobranchs, ophiuroids and crustaceans are also commonly found in association with sponges, and the disappearance of the latter would automatically reduce the specialized associated invertebrate biodiversity.
