It has been speculated that wood material does not degrade in the extreme cold waters of Antarctic14,17. However, we show that this assumption is not correct as we found active specialized lignocellulolytic fungi and bacteria degrading the wood cell walls of long-term submerged material. Further microbial activities in the wood was prevented as the samples were stored 50% alcohol after they were collected in 2010.
The anthropogenic wood samples of Douglas fir retrieved at two different sites outside McMurdo station showed ongoing microbial decay in both samples after 50 and 36 years of exposure at approximately 20 m depth. The two samples showed similar decay profiles dominated by an extensive decay by soft rot fungi in the outermost 2–4 mm of the board (Figs. 1, 2, 3, 4) accompanied by discrete attack of tunneling bacteria (Figs. 5, Suppl Fig. 3). No other types of wood decay were observed. The SR hyphen could be correlated to individual SR cavities (Figs. 1a, b, 4b) and TB were found in their characteristic burrows (Fig. 5a, b). Both features are indicative of ongoing degradation.
The history of the two wooden boards were different and it is not known whether the gangplank could have been infected and degraded during its presumable long time on board a ship. In contrast, the construction board was new and sound when it was used in an underwater/seabed construction; therefore it was not degraded at the start of exposure. When our analyses showed that both boards were degraded to an almost equal extend and had the same decay profile it strongly suggest that that gangplank did not have any “pre-infection” of importance. This conclusion is supported also by the fact that both boards were made by the same wood species (Douglas fir), exposed in the same waters at a similar depth, and for a comparable amount of time. We therefore conclude that decay observed in both boards is a consequence of marine seabed exposure in the water of McMurdo.
The SR decay pattern was very distinctive (Figs. 1, 2, 3, 4) and matched with morphological features typical of SR, type I, found in both marine and terrestrial environments12. The SR type I is characterized by an initial hyphal infestation in the lumen followed by penetration and growth within the secondary cell wall that is rich in holocellulose. Hyphen follows the orientation of the microfibrils, which results in characteristic helical elongated SR cavities formed during decay19,20,21. Marine SR decay are generally often concentrated in the outermost layers of the surface, as observed in baits exposed to diverse seas in an international study22, and shipwreck timbers23,24. The wood surface will soften and often darker6.
Two features might stand out for Antarctic SR decay. These are (1) the decay rate, and to a lesser extend (2) the thickness of the hyphen and cavities produced by the fungi. Compared to decay rates of wood exposed in other marine waters, a penetration of 2–3 mm in 35-, respectively 50 years represents extremely slow activity. Comparable data from saline marine trials at the British coast shows between 1 and 2.4 mm penetration of SR fungi after only 40 weeks of exposure (about 3 mm/year) and a weight loss about 30% in pine samples25. This is supported by laboratory studies running for 24 weeks where up to 25.9% dry mass loss was evident after decay test of 14 marine SR isolates26. This means that annual decay rate about 0.05 mm/year at McMurdo compared to 3.0 mm/year at the British Coast is almost two orders of magnitude slower in the Antarctic. This correlates with the unpublished slow bacterial growth rates observed in McMurdo Sound at 43 m in 1989 (J. Hansen & P. Dayton, personal communication). The second feature; the very thin and closely aligned SR cavities (Figs. 2, 3), could be a response to adaptation in an extreme environment. Morphological change and de-sizing of microorganisms have been described in energy poor environments were “maintenance state” and “survival state” are suggested 27.
TB are cosmopolitans and ultimate wood degraders, as they do degrade preservative treated wood, as well as very durable timbers in aquatic as well as in terrestrial environments20,28. The identity of these rod-shaped bacteria are still not known. The morphological decay features of the chamber forming TB (Fig. 5a, b) were in principle identical to those found in earlier SEM (scanning electron microscopy) studies on TB23,29,30,31,32. However, the chambers appeared extremely narrow, which might indicate a more repressed growth in the Antarctic waters. Further details on the TB decay process on a cellular level are given in TEM (transmission electron microscopy) studies20,33.
We found TB degradation taking place close to SR decay and occasionally within the same fiber. This is a common observation in marine trials, but not often reported. A long term experiment at the west coast of Sweden showed that both SR and TB were simultaneous degrading wood (pine, oak and birch) after only 6 and 12 months in the water column34. Decay decreased 10 cm below seabed and only erosion bacteria were found able to degrade wood in the anoxic sediment layers at 48 cm depth. This emphasizes the need of dissolved oxygen for growth by SR and TB; something that was available in the waters of Antarctic, where concentration of oxygen are close to saturation reflecting the annual phytoplankton blooms35.
Inside the wood material, at the boundary zone where degraded and still non-degraded tissue meet (Fig. 3a), initial decay by SR fungi was the only evidence of microbial life. In contrast, a large numbers of secondary bacteria and/or scavengers were present in the heavily degraded fibers from the surface area (Supplementary Fig. 4 a, b). Some had spectacular forms, like the twisted short rods and the screw/spiral-formed. The latter have also been observed in submerged timbers from the shipwreck Defence on the east coast of US.36. These observations confirm that the microbial community associated with wood degradation increases in size and diversity as decay by primary degraders (SR, TB) proceeds8,33. Recent complementary and in-depth information from DNA analyses on wood falls at varying depths reports on complicated ecosystems and significant bacterial diversity and succession within the wood surface after relatively short time of immersion 37,38,39,40. Similar type of data would be most interesting from the Antarctic region.
The global spread of marine fungi is mainly related to the temperature and salinity of the water as well as the depth. Some temperate- and tropical seas contain many lignicolous species whereas the Antarctic seas have very few species. This could related both to the extreme environment as well as to the fact that this area has been less explored by scientists41. In 2000, a large number of lignicolous marine fungi were tested in laboratory experiments for evidence of active wood decay. Out of 84 species, a total of 30 did form soft rot decay (Ascomycota, Mitosporic (Fungi Imperfecti), and 2 species white rot decay (Basidiomycota)11. The still most comprehensive list, containing 59 marine soft rot producing fungi are given by Mouzouras in 1989, although some species have been added during the last 40 years and more await identification42. The Soft rot fungus degrading the wood from Antarctic may represent novel species. No previous soft rot decay has been reported from Antarctic waters, but there is evidence of a few lignicolous fungi. In 1985, lignicolous fungi was isolated from the waters of sub-Antarctic Signy Island and two fungi were dominant; Monodictys pelagica (T.W. Johnson) E.B.G. Jones, 1963) and Ceriosporopsis tubulifera ((Kohlm.) P.W. Kirk ex Kohlm., 1972) 15. Both species are today listed as typical marine soft rot degraders in a variety of waters 11,21. M.pelagica have a wide salinity tolerance 43 and an extensive distribution in oceans and described among the most common fungi imperfecti in the northern colder waters 44, although it also is observed from the southern hemisphere at the cold waters of Chile 45. M. pelagica has also been identified as serious degraders of timbers from the historic warship Mary Rose, UK as well as potential degrader of shipwrecks in the Baltic Sea6. Ceriosporopsis tubulifera have been reported from the Arctic region46.
Our examination of McMurdo wood samples has demonstrated activity and growth of lignocellulolytic soft rot fungi and tunneling bacteria in the cold Antarctic waters. For wood material and wooden shipwrecks situated in these waters the absence of marine borers prolong the lifespan of this organic material. But as shown, a slow microbial deterioration takes place and will continue over time until wood is totally decomposed. This situation is in many aspects similar to the degradation process observed in the brackish Baltic Sea, where many unique historic shipwrecks are found seemingly well preserved by marine archaeologists47. Here, analyses have shown decay by both SR, TB, and erosion bacteria and a slow transformation of solid wood takes place, leading to a continuous breakdown of the surface layers6,24,48,49. For the historic ships including Nordenskjold’s Antarctic that sank in 1902 and Shackleton’s Endurance that sank in the waters of Antarctic in 1915, decay processes might be slightly slower, as the rate observed are around 3 mm/ 50 years, compared to soft wood from the Vasa wood that are more than 20 mm/300 years (3.3 mm/50 years). But decay rates are complicated because they are found to be dependent on several factors, some related to the wood itself, others to environment, and finally to the time of exposure6.