Host age is not a consistent predictor of microbial diversity in the coral Porites lutea

Abstract

Corals harbour diverse microbial communities that can change in composition as the host grows in age and size. Larger and older colonies have been shown to host a higher diversity of microbial taxa and this has been suggested to be a consequence of their more numerous, complex and varied micro-niches available. However, the effects of host age on community structure and diversity of microbial associates remain equivocal in the few studies performed to date. To test this relationship more robustly, we use established techniques to accurately determine coral host age by quantifying annual skeletal banding patterns, and utilise high-throughput sequencing to comprehensively characterise the microbiome of the common reef-building coral, Porites lutea. Our results indicate no clear link between coral age and microbial diversity or richness. Different sites display distinct age-dependent diversity patterns, with more anthropogenically impacted reefs appearing to show a winnowing of microbial diversity with host age, possibly a consequence of corals adapting to degraded environments. Less impacted sites do not show a signature of winnowing, and we observe increases in microbial richness and diversity as the host ages. Furthermore, we demonstrate that corals of a similar age from the same reef can show very different microbial richness and diversity. Corals contain diverse and complex microbial communities that play critical roles in maintaining and promoting host fitness and survival 1-3. They are involved in nutrient cycling 4 , and help prevent colonization by pathogenic microbes through the occupation of potential niches 5 and the production of specific antibacterial compounds 2. These communities can differ over space and time, among host species, and with environmental perturbations 6-9. Yet, some coral-associated bacterial communities remain constant with no discernible temporal changes 10,11. These contrasting patterns demonstrate some of the challenges faced when attempting to understand the coral microbiome. Numerous studies show that host-associated microbes can and do differ over comparatively small spatial scales 7,12-14. However, few have explicitly examined how host age affects the microbial community, and those that have are limited by colony size as a proxy to obtain a crude estimate of age 15,16. These studies show conflicting patterns with one reporting a steady, yet significant decrease in bacterial diversity with increasing size 16 , while the other demonstrates a general stepwise increase in bacterial diversity with increasing size followed by a slight decrease in diversity of the largest and assumed oldest corals 15. However, it should be noted that the latter study by Williams et al. 15 is limited by the young age of the assumed oldest corals, which have been estimated at only 10-12 years old. Pollock et al. 16 suggest that early coral recruits and larvae have more diverse microbiomes in comparison to later life stages, which is consistent with previous work suggesting that a 'winnowing' of the mic...

The Microbiome of the Reef Macroalga Sargassum ilicifolium in Singapore

“…Our analysis shows a differentiation in the microbial communities associated with the structures sampled, with the holdfast harboring the most distinct community. This is in line with studies performed on other marine organisms from the region, which have shown microbial community divergence over small spatial scales in seagrasses, mangroves and corals [32][33][34]; the same S. ilicifolium structures have also been shown to harbor distinct fungal communities in Singapore [39]. Like other studies examining algal associated microbiota, we show that holdfasts and leaves contain a large proportion of Alphaproteobacteria and Gammaproteobacteria; however, noticeable by their absence in both of these structures, samples collected in Singapore do not contain the class Flavobacteria in comparison to those collected from temperate environments [6].…”

“…Research examining the macrophyte-associated microbiome shows that microbial communities associated with different tissues or plant structures contain different communities, likely a consequence of the different roles different parts play in promoting host survival [ 29 , 30 ]. These communities can also be significantly different even over relatively small spatial scales, such as less than 10 km in some cases [ 31 , 32 , 33 , 34 ]. Photophysiological and biochemical heterogeneity between structures has been documented for Sargassum spp., with differences in photosynthetic rates [ 35 ], phlorotannin content [ 36 ] and C:N ratios [ 37 ] being reported.…”

Spatial and Structural Factors Shape Seagrass-Associated Bacterial Communities in Singapore and Peninsular Malaysia

“…However, work is now challenging the notion that variance is low in microbial communities, and congruent with other research examining marine microbiomes (Cúcio et al, 2016;Crump et al, 2018;Bay et al, 2020;Osman et al, 2020;Tan et al, 2020;Wainwright et al, 2020) we show that bacterial communities can be significantly different between sampling location and structure examined, and this spatial variance is particularly strong in sediment samples in comparison to living seagrass structures. This is consistent with previously proposed hypotheses suggesting that habitats offered by living plant organs (i.e., leaf, fruit, etc.)…”

The Mangrove Microbiome of the Malay Peninsula

“…As climate change progresses and coastal habitats are further degraded by land use changes, eutrophication, and other anthropogenic activities, many of these coastal ecosystems are predicted to become net sources of carbon instead of sinks as microbial communities change in response and sequestered carbon becomes available for microbial cycling [17,[19][20][21][22][23][24]. Consequently, mangroves and other coastal habitats, along with their associated blue carbon stocks, are unlikely to fulfil their claimed potential as nature based climate solutions, and many of their benefits are likely overstated [15,[25][26][27][28] The importance of the microbiome in maintaining and promoting host health has been recognised in many organisms in both terrestrial and marine environments [29][30][31][32][33], and the role of the microbiome in promoting plant growth and resilience in terrestrial plants is well established [34,35]. However, the ecological importance of the coastal microbiome is not yet well-understood, although several studies have shown that fungal and bacterial diversity are key to habitat restoration in marine environments [5,8].…”

“…The importance of the microbiome in maintaining and promoting host health has been recognised in many organisms in both terrestrial and marine environments [29–33], and the role of the microbiome in promoting plant growth and resilience in terrestrial plants is well established [34, 35]. However, the ecological importance of the coastal microbiome is not yet well-understood, although several studies have shown that fungal and bacterial diversity are key to habitat restoration in marine environments [5, 8].…”